THE ICAC RECORDER
International Cotton Advisory Committee
Discover Technical Natural Information Section
Fibres VOL. XXXV No. 2 Initiative JUNE 2017
Update on Cotton Production Research
JUNE 2017 3
Contents Pages Introduction...... 3 Beware of the Boll Weevil, Bollworms, Whitefly and Leaf Curl Virus...... 4 Dr. David Matthias Stelly, Winner of the “2017 ICAC Researcher of the Year Award” ...... 30 International Cotton Researchers Association (ICRA): Updates on Major Activities...... 31 ACRDN VII Meeting...... 32 ALIDA XIV Meeting...... 32
Introduction
This issue of THE ICAC RECORDER has a technical article, in India and partly in Pakistan, whiteflies and leaf curl virus authored by Keshav R. Kranthi. It deals with immediate and proliferated in ecosystems saturated with the newly approved impending threats of boll weevil, bollworms, whitefly and susceptible Bt-cotton hybrids/varieties. Whiteflies developed leaf curl virus to cotton production systems in major cotton resistance to almost all recommended insecticides due to growing countries. In addition to the technical article, a brief repeated and indiscriminate use. Outbreaks followed soon. note from Dr Michel Fok, Chair of the International Cotton Recently, pink bollworm infestations have been causing Researchers Association (ICRA) provides an update on recent serious economic losses because of resistance to Bt-cotton in ICRA happenings. THE ICAC RECORDER is please to India and Pakistan. Reports of Bt-resistant-Helicoverpa spp., present a brief biographical sketch of Dr David Stelly, ICAC in USA, China, India and Pakistan are also causing concerns. Researcher of the Year 2017. Thankfully, there are some remedies and solutions reported Recent research publications indicate that there are at least in scientific literature. However, many of these are not five biotic-threats in the five major cotton growing countries, immediately around the corner. Biotech Bt-cotton expressing India, China, USA, Pakistan and Brazil which need to be VIP3A is a possible next-gen remedy that is now available taken seriously to prevent yield losses and to arrest a possible for use, but how long and how effectively it would keep decline in global cotton production. The five major problems Helicoverpa spp., at bay remains to be seen, especially in are represented in the newly discovered cotton bollworm light of bollworm resistance to the Cry1 and Cry2 proteins. Helicoverpa armigera (Hübner) species in South America; the Recent scientific publications report a few other novel biotech pervasive presence of the notorious boll weevil in Brazil; the cotton technologies for the control of boll weevils, whiteflies, Bt-resistant pink bollworm, the highly invasive insecticide- CLCuD and bollworms. Unfortunately, these new biotech resistant whiteflies and the intractable cotton leaf curl virus products may take a few more years to complete biosafety disease (CLCuD) in India and Pakistan; and the impending assessment and field evaluation before they are approved for problem of Bt-resistant Helicoverpa species in USA, China, commercial cultivation. India and Pakistan. The increasing level of pesticide usage Pest management becomes fragile and more challenging in these countries over the recent past is a pointer towards when worms become resistant to Bt-proteins and insecticides. the rising levels of pest infestation. These pests pose serious In the absence of a robust arsenal of scientifically developed threats to cotton production and cannot be ignored. Except tools, these pests can potentially recreate the nightmarish the newly found H. armigera in Brazil, the other insect pest situation of the yester years. New insecticides are available, and disease problems are not new to these countries. All five but the worms have a history of winning the battle hands problems are recalcitrant and the countries are aware of this. down when confronted with chemicals. The current desperate Until about a few years ago, whiteflies and CLCuD were kept predicament of having to deal with the monstrous boll under control in India and Pakistan, with a combination of new weevils, the insecticide resistant whiteflies, the incurable leaf insecticides and tolerant cultivars developed by public sector curl virus and the Bt-resistant bollworms, steers the roadmap institutions, whereas bollworms were effectively controlled back again towards IPM. Why IPM? Will IPM deliver now by biotech Bt-cotton. But the overconfidence of rapid when it was considered to be unsuccessful in yester years by deployment of biotech cotton in a multitude of new cultivars, several researchers? The fact is that there is no alternative as while ignoring the basic tenets of integrated pest management of now except to look at holistic options that can lend long (IPM), allowed the worms to return with vengeance. Mostly term sustainability to pest management. All such roads lead
The ICAC RECORDER (ISSN 1022-6303) is published four times a year by the Secretariat of the International Cotton Advisory Committee, 1629 K Street, NW, Suite 702, Washington, DC 20006-1636, USA. Editor: Keshav R. Kranthi
In the last ten years, five countries, India, China, USA, Pakistan enhancement that may take place, especially in the five major and Brazil together constituted 72 to 76% of the global cotton cotton producing countries. area annually and contributed to more than 75% of the global cotton production each year. In the recent past, there The Five Major ‘Biotic-Stress’ have been clear signals from research publications that pest Challenges problems are brewing up in these top five cotton producing countries. These insect pests are notorious. Concerted efforts The five major cotton growing countries are now plagued are required to address the problems at the earliest before they with either new insect pests or with Bt-resistant bollworms become more serious. The boll weevil, cotton bollworm, pink or herbicide resistant weeds and increasing pesticide usage. bollworm, whitefly and leaf curl virus are known to cause Incidentally, in all the five countries, the major yield-limiting heavy economic crop losses and are difficult to manage. factors are biotic threats. These relate to insects and an insect Needless to state, changes in production of the five countries transmitted disease. will impact global production proportionately. The most serious threats are: The past ten years were characterized by global yield • The boll weevil, Anthonomus grandis (Boheman) and stagnation and trends towards increasing chemical usage. the cotton bollworm, Helicoverpa armigera (Hΰbner) in Increase in pesticide use during this period indicates the Brazil; increased levels of attention drawn by insect pests and an • The whitefly, Bemisia tabaci (Gennadius), the leaf curl insect-vector transmitted disease. Yields reached a plateau in virus and the Bt-resistant pink bollworm, Pectinophora India, USA, Pakistan and Brazil over the past 10-12 years, but, gossypiella (Saunders) in India and Pakistan; have been on the ascent consistently during the past several years in China. Though, everything looks deceptively normal • Helicoverpa zea (Boddie) in USA and impending threat as of now, the different undercurrents of biotic threats in the of Bt-resistance in H. armigera in India, Pakistan and five major countries can potentially destabilize cotton yields China. in the near future, if unattended to. One of the major concerns The problems are very serious and so is the potential threat to is that, while insect pest infestation levels in major cotton cotton production systems growing countries continue to increase, new technologies to The threats are being addressed efficiently by some countries, control them do not seem to be in place. This is reflected in while others react only when the problem gets worse. While the data of yield stagnation and increases in pesticide use that some countries are aware of the incoming risks, others may happened despite the introduction of new technologies such have only perceived some initial indications of the possible as improved varieties, new biotech products and new potent implications. Outstanding research and administrative pesticides during the past ten years. Will the major countries efforts in USA paved the way for successful planning be able to effectively combat the imminent biotic threats? and implementation of effective programs on area-wide Can the yields increase hereafter as we move towards 2020? management of whiteflies, bollworms and boll weevils. These Are there technologies at hand now, or short-listed for the insects would have otherwise caused heavy economic losses near future to prevent decline in yields or to enhance yields, to cotton production in the country. The problem of boll weevil reduce chemical usage and bring down the cost of production? in Brazil and the impending threats of bollworms in India, The answers to these questions will largely depend on the Brazil, Pakistan, USA and China deserve more attention in technological changes related to pest management and yield these countries. Incidentally, India, China, USA, Brazil and JUNE 2017 5
Table 1. Biotic stress factors in the 5 major cotton growing countries
Insect pest / disease USA Brazil China India Pakistan 1. Boll weevils ***** 2. Bt-resistant bollworms a. Pink bollworm * ** ***** *** b. Helicoverpa & Heliothis spp. ** * ** *** ** 3. Whiteflies * ** ** **** **** 4. Leaf curl virus disease ***** *****
*Number of asterisks indicate intensity of the threat, as surmised from research papers
Pakistan are the largest users of insect-resistant biotech cotton gene cry10Aa was developed in Brazil and was reported to be technologies. In addition to the insect-resistant biotech cotton, highly effective in controlling the boll weevil (Ribeiro et al., USA and Brazil have also been the major users of herbicide 2017). A few other biotech-cotton based technologies were tolerant cotton. Interestingly, all the five countries are almost also reported recently (Silva et al., 2015, Macedo et al., 2017, completely dependent now on biotech traits in their cotton Araujo et al. 2005 and Medel et al. 2015). These technologies varieties. But, technologies have a life of their own. They add new dimensions to the existing boll weevil management are seldom expected to continue to remain effective forever. arsenal. To ensure long term sustainability and profitability Over the recent past, researchers across the world have been of cotton production systems in South America, cotton IPM constantly issuing alerts on the declining efficacy of the biotech programs must incorporate essential ingredients of boll traits in many countries due to either bollworm resistance to weevil eradication program, coupled with the new biotech- Bt (Bacillus thuringiensis) proteins or the development of cotton technologies that target boll weevils and bollworms. herbicide resistant weeds. Another concern is the emergence The incidence of pest and disease attacks is high in Brazil, since of minor pests as major threats to production systems. most of the land used for cotton is in a tropical climate that is Mostly these are insect pests that are not affected by Bt- conducive for pests. High humidity attracts fungal diseases. proteins. Consequently Bt-resistant bollworms and the newly Some of the important biotic stress elements are nematodes, emerging pests lead to increases in pesticide applications. fungal diseases, boll weevil, Anthonomus grandis (Boheman), Publications indicate that researchers are working out the pink bollworm, Pectinophora gossypiella (Saunders), tobacco best possible solutions to combat the biotic stress problems in budworm, Heliothis virescens (Fabricius), cotton bollworm their respective countries. These technologies are in various Helicoverpa armigera (Hübner), cotton leaf worm, Alabama stages of development. It remains to be seen whether they will argillacea (Hübner), fall armyworm, Spodoptera frugiperda succeed in time to prevent a negative impact on global yields. (J.E. Smith) and whitefy, Bemisia tabaci (Gennadius). Boll This article attempts to evaluate the risks and examine the weevils pose the most formidable threat with potential to cause recent scientific advances that reflect hope for the future, and complete damage if left unchecked. The cotton blue disease potential remedies that are at various stages of development in caused by aphid transmitted luteoviruses is yet another threat each of the five countries. that looms large if left unattended. The Boll Weevil in Brazil Farmers are inclined to use insecticides as the main remedial measure for insect pest control, thereby rendering the systems The boll weevil has been one of the menacing factors in highly chemical intensive. Helicoverpa armigera can easily the whole of South America starting from the mid 1980s. emerge as a major pest in Brazil and elsewhere in South Grubs of the weevil feed inside the developing bolls. This America due to indiscriminate use of synthetic pyrethroids, as cryptic feeding habit of boll weevil is the main hurdle in was the case in other countries across the world. The arrival of pest management. Boll weevils can cause severe economic the boll weevil in the mid-1980s and the bollworm Helicoverpa losses up to 100% in the absence of management. Adults armigera in 2012-13, tilted the balance enormously towards start colonizing cotton at the time of squaring. They feed on chemical dependence. At least one-third of insecticide usage squares, flowers and oviposit inside them causing complete is directed towards boll weevil control. High use of fertilizers, damage due to abscission. Boll weevil grubs reside and feed especially in an unbalanced manner, can aggravate pest and inside fruiting parts and thus are not vulnerable to naturally disease problems. Repeated applications of insecticides early occurring predators, parasitoids and pesticide applications. in the season, mainly for aphid and boll weevil control, disrupt Thus far, the main methods of boll weevil management are the ecosystem severely to prompt resurgence and emergence based on cultural control, pheromone traps and insecticide of a series of insect pests, including mites, aphids, whiteflies applications to break reproductive cycles and diapause. Very and bollworms, thereby necessitating further repeated recently, a new Biotech-cotton technology expressing the Bt- applications of insecticides. A substantial portion of about 6 ICAC RECORDER
80% of the cost of cultivation at US$ 2,500 per hectare in mortality in boll weevils and 40% mortality in the fall army Brazil is towards agrochemicals (Barbosa and Ramos, 2014). worm with severe growth regulating effects in the surviving Recent reports suggest over-dependence of cotton cultivation larvae. These scientific advances signal new hope for boll on pesticides. Historically, indiscriminate use of pesticides weevil management. has invariably caused a decline of cotton production systems New genes were identified for use in the development of across the world. Currently, Brazil is facing a huge challenge biotech cotton varieties. Navas et al. (2014), identified two and needs to develop integrated Pest Management (IPM) Cry proteins Cry8Pa3 and Cry8QA2 from a Bt strain INTA systems through judicious pesticide applications for effective Fr-7-4, that were toxic to Anthonomus grandis. Oliveira et pest control while ensuring sustainable ecology and a healthier al. (2011) developed a mutant protein Cry8Ka5 with high environment. At this point in time, only IPM can orient cotton levels of median leathal concentration LC50 toxicity at 2.83 towards sustainability. ppm. Macedo et al. (2017) reported that gene silencing of Barbosa and Ramos (2014) clearly emphasize the need for chitin synthase2 through ribonucleic acid interference (RNAi) initiatives towards the development of sustainable cotton caused 100% mortality of the boll weevil. They also reported programs. “Today, cotton growing in Mato Grosso, West that gene silencing caused inhibition of oviposition by 93%. Bahia and elsewhere in the Cerrado is a extremely high-input The results create a new promise for the development of activity with the costs to produce one hectare surpassing biotech cotton expressing dsRNA (double stranded RNA) 2,500 US$.....Because the uncontrolled high use of modern of AgraCHS2 (Anthonomus grandis chitin synthase 2) for inputs in cotton growing, considering their side effects on boll weevil management. Previously, based on transcriptome the economy, on human health and on the environment, may studies of mid-gut genes, Firmino et al. (2013) had reported not be sustainable over the long run, caution must be taken effective growth regulating effect with gene silencing of chitin against their overuse. What should count in the future is not the synthase through RNA interference. A few papers (Araujo et number of cotton bales in the barn but the number of dollars al., 2005 and Medel et al., 2015) also indicate that protease in the farmer’s pocket after all the costs are paid for, with due inhibitors had detrimental effects on weevils. It may be concern to human health and the environment. Uncertainties interesting to evaluate the Cowpea trypsin protease-inhibitor on future cotton marketing trends and a growing concern on (CPTi) expressing biotech-cotton varieties developed by the consumers in relation to the use of out-of-the-farm inputs, Chinese Academy of Agricultural Sciences (CAAS), China, cotton farmers associations, universities, and research & for their toxicity to boll weevils. extension systems must joint efforts and develop more benign Identification of novel Bt genes such as cry1Ia and cry8 for and more sustainable cotton production methods to guarantee boll weevil control, coupled with the promise of protease the sustainability of this very noble activity over the years to inhibitors and RNAi (Ribonucleic acid interference) based come.” gene silencing of chitin synthase genes, provide additional Recent Exciting Research Advances options for the development of new highly potent biotech cotton varieties by combining these with the newly developed At least three promising ‘boll weevil-resistant’ biotech Bt- Cry10Aa protein based biotech cotton varieties. Also, cotton varieties were developed in Brazil in the past two years. pyramiding the Cry10Aa biotech cotton event with the A recent paper ‘Transgenic cotton expressing Cry10Aa protein currently available bollworm-resistant biotech cotton events confers high resistance to the cotton boll weevil’ in Plant expressing other Cry proteins such as Cry1Ac, Cry2Ab, Biotechnology Journal, by Ribeiro et. al. (2017) generated Vip3A, Cry1F, protease inhibitors (CPTi CAAS event) and considerable excitement for boll weevil management. The RNAi based chitin-synthase silencing events, would result Brazilian scientists reported successful transformation of in robust biotech varieties that can combat the boll weevil a Brazilian cotton cultivar (BRS 372) with cry10Aa gene and bollworms more effectively. The multi-gene biotech derived from Bacillus thuringiensis subsp. israelensis (Bti) cotton varieties can be valuable components of sustainable strain using particle bombardment method. The Cry10Aa integrated pest management (IPM) to keep the boll weevil and protein was found to be highly toxic to Anthonomas grandis bollworms under control for the longest possible time. (Aguiar et al., 2012). The biotech plants were found to express the Cry10Aa protein at 3.0 to 14.0 ppm, in leaves and flower Bt-Resistant Pink Bollworms in buds adequate to cause up to 100% mortality of the grubs and adults of the boll weevil. The biotech cotton variety presents India and Pakistan a great opportunity for boll weevil management. Previously The pink bollworm, Pectinophora gossypiella (Saunders) Silva et al. (2015) had reported the development of biotech (Lepidoptera: Gelechiidae), is one of the major concerns now cotton variety BRS 293 using Cry1Ia that could cause 56.7 to in India, Pakistan and China. The pink bollworm developed 83.7% mortality of boll weevils and 88.1% mortality of the resistance to Bt-cotton in India recently and has been causing fall army worm Spodoptera frugiperda. Oliveira et al. (2016) significant damage to the crop over the past two to three years developed a Bt-cotton variety BRS Cedro using Cry1Ia12 (Kranthi, 2015). Though pink bollworm is a major pest also through pollen tube pathway method and reported up to 60% in the USA, implementation of effective monitoring and JUNE 2017 7 management programs using pheromones and release of bollworm is a pest of long-season cotton. Historically cotton male sterile moths (Simmons et al., 2011; Morrison et al., varieties in India, Pakistan and China were of long duration. 2012; Tabashnik et al., 2012), refuges and appropriate gene The pink bollworm feeds on cotton, bhendi (okra), Hibiscus, pyramids (Head and Dennehy, 2010) ensured that the pest and jute. Infestation starts in early winter and continues for is still under control and resistance development is delayed. 4-5 months depending on the availability of host crops. Moths Cry1Ac is highly toxic to the pink bollworm (Mohan et al., are dirty brown in colour and about 5 mm in length. Eggs 2015). Bt-cotton expressing Cry1Ac was able to control pink are laid mainly on floral parts or young bolls and hatch in bollworm very effectively until the worm developed resistance 3-4 days. Within two days of hatching, the young larvae bore to Cry1Ac in India (Dhurua and Gujar, 2011; Ojha et al., inside flowers or young bolls. Larvae turn pink in colour soon 2014; Mohan et al., 2015), China (Wan et al., 2012; Tabashnik after feeding on tender seeds. Larvae feed on developing seeds et al., 2012) and Pakistan (Akhtar et al., 2016). Pink bollworm thereby damaging bolls and leading to premature boll opening resistance to Cry1Ac in Bt-cotton grown in the central Indian or rotting. Infested flowers get ‘rosetted’ and twisted. Fibre state of Gujarat was first recorded in 2009 (Dhurua and Gujar, quality in the infested bolls is badly affected due to secondary 2011). Surveys conducted by ICAR-CICR (Central institute fungal infection and staining. Transportation of seed cotton for cotton research, India) in 2014, 2015 and 2016 clearly containing pupae or moths spreads infestation. Ginned and established that pink bollworm larvae were able to survive baled cotton is unikely to harbour live larvae or pupae that on the two-gene cry1Ac+cry2Ab based Bollgard-II (BG-II) would be able to survive and infest new areas. Pink bollworm Bt-cotton hybrids. The surveys showed that about 40-80% of enters into a diapause for 6-8 months. Long duration crop the bolls were found to contain surviving larvae. Resistance allows multiple cycles of the pest which gets carried over into monitoring conducted with larvae collected from Gujarat state the next season. Experience across the globe shows that longer showed that pink bollworms developed resistance to Cry1Ac, the cotton crop duration, higher is the probabilty of potential Cry2Ab and Cry1Ac+Cry2Ab proteins (Chinnababu et al., damage by pink bollworms in the subsequent crop season. unpublished). Subsequently, pink bollworm damage was Potential losses due to pink bollworms were estimated to be reported from central and south India, mostly from irrigated 61% in the USA (Schwartz, 1983), 20.2% in India (Agarwal regions, where Bt-cotton was grown as a long-duration crop. and Katiyar, 1979), 17-26% in China (Luo et al., 1986) and Recent reports from India (Chinnababu Naik, CICR,personal 10.7% in Sudan (Darling, 1951). communication & Kranthi, 2015) unequivocally confirm the Generally, pink bollworms cause maximum economic development of pink bollworm resistance to the dual gene Bt- damage late in the season, which coincides with post-130 cotton expressing the two Cry proteins, Cry1Ac+Cry2Ab. days old crop in many countries. Pink bollworm moths prefer Pink bollworm with its Indo-Pak origins is considered as oviposition on 10-20 days old bolls mostly and seldom cause a traditional pest in the Indian sub-continent. It was first fresh infestation on older or mature bolls. Therefore a short described in 1842 as a cotton pest in India (Ingram 1994). Prior season crop of 150-160 days duration can be cultivated in a to its scientific nomenclature as Pectinophora gossypiella specified time-window of the cropping season to escape pink (Saunders), the insect was known as, Depressaria gossypiella bollworm infestation by creating a mismatch between the boll (Saunders), Ephestia gossypiella (Saunders), Gelechia maturation and seasonal peaks of the pink bollworm. Early- gossypiella (Saunders), Gelechiella gossypiella (Saunders), sown short duration crop is likely to attract pink bollworms and Platyedra gossypiella (Saunders). Generally the pink slightly during the flowering period, but, this peak is small and can be managed. However, the first picked cotton of early sown crop would in all likelihood escape pink bollworms, more so if the variety is of short or medium duration. Late- sown crops of medium and late duration varieties suffer the most. Staggered flowering phase in a continuous manner over an extended period also creates a long vulnerable window for pink bollworm attack. Some varieties may have morphological features of boll rind and allelochemical factors which may be more congenial for pink boll worm infestation thereby resulting in more damage compared to others. Excessive application of nitrogen and irrigation during the vegetative phase results in extended phase of the crop and stretches the crop duration further, wherein the staggered boll formation phase coincides with pink bollworm infestation. The pink bollworm larvae feed on the developing seeds inside devloping green bolls. Therefore, they are not amenable for Fig.1 Pink bollworm Pec�nophora gossypiella damaging a boll insecticide control. However, good pest control is achieved with the use of contact poisons such as the synthetic 8 ICAC RECORDER pyrethroids (Sabry et al., 2014), mainly because of the contact conditions for pink bollworm infestation and allowed toxicity to moths. Subsequent to the introduction of synthetic multiple cycles of multiplication. It was not very pyrethroid insecticides in the early 1980s, pink bollworm was uncommon in India, mostly in the irrigated regions, effectively controlled and was replaced by the cotton bollworm to find the crop being extended up to 8-10 months. Helicoverpa armigera in many countries. The change Excessive use of nitrogenous fertilizers, coupled with happened due to high susceptibility of pink bollworms and application of a few organophosphate insecticide rapid development of H. armigera resistance to pyrethroids. sprays such as monocrotophos and acephate led to Other factors that influenced the pest-shift were, slightly extended vegetative phase and staggered flowering. This hastened crop maturity due to pyrethroid sprays, and disruption provided a continuous source of flowers and bolls as of the ecology of naturally occurring biological control that food supplies, almost all through the year and facilitated had otherwise kept the cotton bollworm populations much pest-multiplication in overlapping generations that were below the economic threshold levels. Indiscriminate use of subjected intensive selection pressure of Cry proteins, pyrethroids also caused severe resurgence of whiteflies. Thus, thus accelerating resistance development (Kranthi 2012). the cotton bollworm and whitefly problems are considered • Large number of Bt-hybrids: Several hundreds of Bt- as a consequence of excessive usage of pyrethroids for pink cotton hybrid varieties were released every year. These bollworm control (Kranthi et al., 2001; Kranthi et al., 2001a; hybrids have variable windows of flowering and fruiting. Kranthi, 2012). Both pests are often referred to as insecticide- These are grown adjacent to each other in the same region induced problems in India. in small-scale farming systems, thereby providing a Causal factors for pink bollworm occurrence and resistance to constant supply of flowers and young bolls as continuous Bt-cotton are listed below: attractants and food sources almost all through the season. 1. Pink bollworm resistance in • Segregating seeds in bolls of China and Pakistan Bt-cotton hybrid plants: In India only F-1 hybrid Bt- cotton varieties were permitted for cultivation. The F-1 Pink bollworm resistance in China and Pakistan is mainly Bt-cotton hybrids are hemizygous for the transgenes. due to the intensive exposure of the insect only to a single Because of which, bolls formed on the F-1 plants Bt protein Cry1Ac and not to a combination of proteins as of single gene based Bt-cotton contain seeds which in other countries. However, resistance development has been segregate in a ratio of 3:1 (Cry1Ac in 3 and none in slow compared to India primarily because both countries 1) for the Cry1Ac protein, and in the two gene based relied on short to medium duration cotton varieties compared Bollgard-II the bolls contain seeds that segregate in the to long-duration Bt-cotton hybrids in India, and also while ratio of 9:3:3:1 (Cry1Ac+Cry2Ab in 9; Cry2Ab alone in India cultivated hemizygous Bt-cotton hybrids, China and 3; Cry1Ac in 3 and none in 1) for the two Bt-proteins. Pakistan opted for homozygous Bt-varieties (Kranthi, 2012). Thus, a single boll contains a mixture of non Bt seeds, Hemizygous Bt-cotton hybrids are those which contain only seeds with Cry1Ac alone, seeds with Cry2Ab alone and one copy of the transgene, unlike the homozygous Bt-cotton seeds with Cry1Ac+Cry2Ab. This situation is ideal for varieties which contain two copies of the transgene. Pink resistance development, due to selection of resistance to bollworm was reported to have caused considerable damage independent proteins. The segregating seeds in bolls of to the single gene cry1Ac based Bt-cotton in Pakistan during F-1 hybrid plants and low expression of Bt-proteins in the 2015-16 cropping season. Pink bollworm resistance to buds, flowers and developing seeds in young bolls allow Cry1Ac was reported to have been one of the main causes for survival of larvae that are heterozygous for the resistant the high level of infestation (Abbas et al., 2016). Additionally, genes, thereby accelerating resistance development. cotton duration increased after the introduction of Bt-cotton in Pakistan (Naveed et al., 2017) and India (Kranthi, 2015) due • Decline in pyrethroid usage: The use of synthetic to which pink bollworm was exposed to multiple cycles of pyrethroids declined in India after late 1990s due to H. selection, thereby accelerating resistance. The pink bollworm armigera resistance to pyrethroids and also due to the caused an estimated loss of US$ 1.2 billion in Pakistan during introduction of Bt-cotton. Decline in pyrethroid usage on the 2015-16 cropping season (Naveed et al., 2017). In China, long duration hybrid-varieties coupled with the presence though a small but statistically significant increase in resistance of non-Bt seeds in bolls of F-1 Bt-cotton hybrids, are of the pink bollworm to Cry1Ac was reported in 2012 in the believed to be the main factors that may have allowed Yangtze River Valley from 2005–2007 to 2008–2010 (Wan et pink bollworms to survive and gradually emerge as a al., 2012) subsequent studies showed that resistance did not major pest on Bt-cotton. increase over the years until 2015 (Wan et al., 2017). • Poor refuge compliance: The compliance of refuge planting of non-Bt cotton was poor (Kranthi et al., 2017). 2. Resistance in India was rapid due to a variety of factors as listed below (Kranthi 2015) Management Strategies • Long season cotton: Extended duration of long season The following IPM strategies are proposed based on the cotton for 160 to 240 days coincided with favourable available literature on the subject: JUNE 2017 9
Pest monitoring Mass trapping Pink bollworm infestation must be regularly monitored using Pheromone traps using gossyplure resulted in 60-80% ‘pheromone traps’ and ‘green boll dissection’ to initiate control reduction of the pink bollworm population in China (Gao interventions at economic threshold levels of 8 moths per trap et al., 1992). Pink bollworm eradication programmes were per night and/or 10% damage in green bolls (Sevacherian and attempted in India (Simwat et al., 1988) but were found to be el-Zik, 1983; Dhawan and Simwat, 1993). expensive. However, early-season use of pheromone at low pink bollworm population densities, coupled with insecticides Resistance monitoring was found to be most profitable (Frisbieet al., 1989). Currently Monitoring the development of bollworm resistance to Bt 20 pheromone traps per acre are being recommended to be set cotton is a key component of management, especially when up early in the season for mass trapping. it alerts the impending restance risk, so that appropriate management strategies can be initiated (Mohan et al., 2015). Mating disruption Gossyplure was used successfully for mating disruption along Biological control with biological control in Pakistan (Ahmad et al., 2001). Pink bollworms are controlled in cotton fields by naturally Pheromone SPLAT technology or PB Ropes can be used occurring Rogas and Apanteles spp. (Singh et al., 1988), effectively for mating disruption (Miller et al., 2015). Chelonus blackburni (Jackson et al., 1979), Trichogramma brasiliense (Tuhan et al., 1987) Trichogramma bactrae Varieties resistant to sap-sucking insects (Malik, 2001) and Trichogramma evancens (Saad et al., 2012). With varieties that are endowed with resistance to sap-sucking Cheema et al. (1980) found 22 parasites of P. gossypiella in pests, it is possible to avoid the use of systemic insecticides a survey in Pakistan: of these, only Apanteles angaleti was such as monocrotophos, acephate, thiomethoxam, acetamiprid, a major parasitoid. Based on practical field experiences in imidacloprid or clothianidin early in the season. Avoidance of India, deployment of biological control using the parasitoid these insecticides helps to conserve the naturally occurring Trichogramma bactrae (Nagaraja) was found to be most biological control for season long pest management and to economical, feasible and effective, especially in the initial obtain synchronous early maturity of bolls which helps in stages of pest infestation. the escape of pink bollworm infestation (Kranthi and Kranthi 2010). Refuge Compliance of refuge planting with 5 to 20% area of non-Bt Insecticides cotton plants in the vicinity of Bt-cotton fields is one of the Synthetic pyrethroids may be used for the control of pink most important strategies to manage pink bollworm resistance bollworm (Sabry et al., 2014) late in the season at economic to Bt-cotton (Kranthi et al., 2017). threshold levels of damage. Spraying pyrethroids early in the season, as insecticide mixtures and in excess at any time in the Avoid extending the crop season must be avoided to prevent outbreaks of H. armigera Termination of the crop immediately after final harvest and whiteflies. without resorting to ratooning or extending the crop through extra irrigation is an important practice to prevent availability F-1 hybrids with homozygous cry genes of the host plants for multiple cycles of the pink bollworm. In countries where Bt-cotton hybrids are used, seed companies Crop termination also helps to reduce the chances for pink must be encouraged to ensure that both parent varieties of the bollworm diapause where the end of diapause is triggered by hybrid are homozygous for the cry genes so that Cry proteins day length (Frisbie et al., 1989). are present in the hybrids in a homogeneous form, instead of the segregating heterogeneous form as in the current F-1 Destruction of crop residues hybrids (Kranthi, 2012). A recent paper (Wan et al., 2017) Cotton stalks habor diapausing and non-diapausing pupae. showed that ‘hybridizing transgenic Bt cotton with non-Bt It is important to destroy stalks to prevent carry-over of the cotton countered resistance in pink bollworm’. The authors pupal stages into the subsequent season. Stalks should be used F-2 Bt-seed to demonstrate that the 25% non-Bt plants chopped and incorporated back into the soil, or used as fuel or served as an effective refuge to delay resistance development. industrial purposes. It is interesting that the proposal is analogous to the existing crop situation in India wherein the bolls on F-1 hybrid Short season crop plants actually contain seeds that segregate in F-2 ratios, but Short duration (140-160 days) varieties, when sown early resistance developed in an accelerated manner. or on time mature before the peak onset of pink bollworm infestation thereby escaping damage. Further, pink bollworm Male sterile release techniques populations get substantially reduced by breaking the pest A large-scale, four-year field deployment of a male-sterile cycles when combined with crop rotation (Beasley and strategy, where refuges are scarce or absent, as in Arizona Adams, 1995). was successful in controlling the pink bollworm. Male-sterile 10 ICAC RECORDER insects were released to mate with resistant pink bollworm in the world, except America. But, with the recent reports of its Bt cotton fields to reduce pink bollworm abundance by >99%, presence in South America, pest management challenges can while eliminating insecticide sprays against the invasive surmount for the entire American region. H. armigera easily pest (Tabashnik et al., 2012a). Such techniques need to be reaches major pest status in many cropping systems because examined for India, Pakistan and China. of a unique combination of four biological characteristics: polyphagy, high mobility, high fecundity, and facultative Recent Exciting Research Advances diapause (Fitt 1989) and due to indiscriminate use of synthetic Pink bollworm continues to be susceptible to Bt-cotton pyrethroids (Kranthi and Kranthi, 2010). despite 20 years of extensive cultivation. The main factors The Heliothine pest complex of cotton bollworms comprises that delayed resistance in Arizona appear to be, timely crop of at least four major species, namely, the cotton bollworm, termination; deployment of abundant non-Bt cotton refuges; Helicoverpa armigera (Hübner), the tobacco budworm, recessive inheritance of resistance; fitness costs associated Heliothis virescens (Fabricius), the corn earworm Helicoverpa with resistance and incomplete resistance (Tabashnik et al., zea (Boddie) and the Australian bollworm, Helicoverpa 2012a). From 2006–2011, refuge abundance was greatly punctigera (Wallengren). Undoubtedly, the first three species reduced in Arizona, while mass releases of sterile pink represent a constant threat to cotton production across the bollworm moths were made, to delay resistance as part of a globe. Amongst the three, the cotton bollworm Helicoverpa multi-tactic eradication program. Sustained susceptibility of armigera is considered to be a monster because it is one of the pink bollworm to Bt cotton in Arizona provided a cornerstone most difficult insect pests to manage. for the pink bollworm eradication program and for integrated pest management in cotton. Reduced insecticide use against Amongst all agriculturally important insect pests, Helicoverpa pink bollworm and other cotton pests has yielded economic armigera has one of the widest distributions, occurring benefits for growers, as well as broad environmental and throughout Africa, the Middle East, southern Europe, health benefits (Tabashnik et al., 2012a) India, central and south-eastern Asia, eastern and northern Australia, New Zealand, and many Pacific Islands (Fitt, The Cotton Bollworm 1989). Helicoverpa armigera moths are known to fly long distances with an ability to disperse widely under favourable Helicoverpa armigera conditions (Pedgley, 1985; Pedgley et al., 1987, Fitt, 1989, The cotton bollworm Helicoverpa armigera (Hübner) was a Colvin, 1990; Riley et al., 1992), Previously endemic to Asia, major problem in China, India, Pakistan and Australia until Africa, Europe and Australasia, it has now been reported in biotech Bt-cotton was introduced into these countries. Recent Brazil (Czepak et al., 2013), Puerto Rico, Argentina (Murúa data show that the worm is adapting to Bt-cotton. Adaptation et al., 2014) and Paraguay and Uruguay (Arnnemann et al., is believed to have slowed due to the deployment of two 2016) with a likely arrival date of between 2006 and 2008 independently acting Cry-proteins, Cry1Ac and Cry2Ab, (Tay et al., 2013; Sosa-Gomez et al., 2015). It is possible that each having a different receptor site in the midgut of the the ability to disperse long distances has helped the species bollworm. Due to intensive planting of Bt-cotton, frequency to establish itself in almost all the cotton growing countries of resistant individuals to Cry1Ac increased from 0.93% in of the world such as China, India, Pakistan, Australia, Brazil, 2010 to 5.5% in 2013 in field populations of H. armigera Uzbekistan, Kazakhsthan, Kyrgyzstan, Brazil, Argentina, from northern China (Zhang et al., 2011; Jin et al., 2015). H. armigera populations in India (Kranthi, 2012; Kranthi, 2015) and Pakistan are showing initial symptoms of resistance to Bt-cotton. H. armigera is known to cause serious economic losses to a wide range of crops including cotton and warrants tremendous efforts to prevent it from causing catastrophic losses to agriculture. The problem can recur again and exacerbate in China, India and Pakistan, once the cotton bollworm develops resistance to Bt-cotton. Very recently, a few years ago, the cotton bollworm Helicoverpa armigera was detected for the first time in South America from Brazil, Argentina, Uruguay and Paraguay. This news rings alarm bells for agriculture not only in South America but also signals a possible invasion into USA. Two related species, Heliothis virescens and Helicoverpa zea are present in USA, but compared to H. armigera, are less devastating in their host range, propensity for insecticide resistance and potential to damage crops. So Fig.2 Co�on bollworm Helicoverpa armigera damaging a bud far H. armigera was ubiquitous in almost all other parts of JUNE 2017 11
Egypt, Burkina Faso, Mali, Mozambique, Myanmar, Sudan, al. 2013). Helicoverpa zea is similarly polyphagous but Tanzania, Morocco, Thailand, Togo, Turkey, Uganda, demonstrates lesser capabilities than H. armigera for damage Vietnam, Zambia, Zimbabwe, Cameroon, Côte d’Ivoire, and resistance development. It is thought to be derived from Greece, Iran, Israel, Kenya, France, Spain and Portugal, with H. armigera founders approximately 1.5 – 2.0 million years the probable exception of USA. ago and the difference in economic damage and resistance Before its current scientific name as Helicoverpa armigera, development may be the consequences of a genetic bottleneck the species was initially named as Noctua obsoleta (Fab.) (Behere et al., 2007). in 1793, after which it underwent a series of nomenclature The pest causes significant damage to cotton and other crops in changes as Chloridea obsoleta (Fab.), Chloridea armigera Asia, Europe, Africa and Australasia, causing losses to crops (Fab.), Heliothis obsoleta (Hubner), Helicoverpa obsolete, estimated at greater than US$ 2 billion annually, excluding (Auct.), Heliothis fusca (Cockerell), Heliothis rama socio-economic and environmental costs associated with (Bhattacherjee & Gupta) and Noctua armigera (Hübner). its control (Tay et al., 2013). In India, crop losses due to H. Although frequently called American bollworm in north Asia, armigera are commonly more than half the yield, and annual it has no connection with the Americas other than the fact losses to cotton and pulses alone have been estimated at US$ that it became an increasingly important pest of a range of 300-500 million (King, 1994). Several estimates of crop Asian crops after the introduction and widespread cultivation losses point out to the enormous magnitude of damage that of American cotton (Gossypium hirsutum) early in the 20th the pest is capable of causing. Sharma (2001) estimated total century (Russell and Kranthi, 2006). global crop losses to this pest at around US$ 5 billion globally, H. armigera lays eggs initially during peak vegetative phase with losses of over US$ 900 million in chickpea and pigeon of the crop, but the damage is minimal due to heavy natural pea in addition to US$ 1 billion spent on insecticides for its mortality of the larvae. Peak oviposition occurs when the crop control. H. armigera caused huge crop losses to cotton with starts producing squares and flowers. About 70-80% eggs are at least four devastating outbreaks that occurred in a cyclic laid generally on the upper canopy and stems, while rest of manner at 3-4 year intervals starting from 1986 to 2001 in the 20-30% eggs are laid on fruiting parts with preference on India, Pakistan and China. During this period, an estimated square and flower bracts. After hatching, the young larvae US$ 8-10 billion worth insecticides were used for its control scrape on the leaf surface before they bore into squares, in India alone (Russell and Kranthi, 2006). About 50% of the flowers and bolls. Larvae prefer fruiting parts to leaves. Each pigeonpea crop was estimated to be lost annually to the pest larva can feed on 8-10 squares/flowers and 2-3 bolls in a in east Africa (Hillocks et al., 2000; Youm et al., 2005). In single life cycle. Typically the larva feeds inside bolls keeping Queensland, Australia, cotton crop losses were estimated to half of its body outside. The larva feeds for two weeks on the be 7.7% despite the expenditure of US$ 4.2 million for its fruiting parts before it turns into pupa. Moths emerge from control (Fitt, 1994). pupae after 7-10 days and start oviposition within 3-4 days. Helicoverpa armigera is known for its strong capability to Helicoverpa armigera is known to feed on an extensive develop resistance to insecticides recommended for its control. range of more than 180 plant hosts from about 45 families, Indian and Chinese H. armigera recorded the highest levels of (Manjunath et al., 1989; Tay et al., 2017) including resistance to insecticides, as compared to any region of the agriculturally important crops such as cotton, chickpea, world. Extensive studies were conducted during the period pigeon pea, peas, cowpea, sunflower, sorghum, groundnut, 1980 to 2000 on insecticide resistance status of H. armigera, field beans, tomato, tobacco, maize (Gowda 2005) in addition mainly in India (Armes et al., 1996; McCaffery, 1999; Kranthi to wheat, okra, castor and a wide range of vegetables. The et al., 2002), China (Shen et al., 1994; Tan 1999), Pakistan species is known for its high propensity to rapidly develop (Ahmad et al., 1999) and Australia (Forrester et al., 1993; resistance to insecticides (Kranthi et al., 2002; Yang et Gunning et al., 1998).
Table 2. Examples of H. armigera resistance factors (x-fold) to insecticides in China, India, Pakistan and Australia
Pyrethroids Organophosphates Carbamates Endosulfan Reference
Armes et al., 1996; Kranthi et al., 2001, India 10 to 26,151 >59 >30 4 to 37 2001a; McCaffery et al., 1989
Mu and Wang, 1995; Shen and Wu, 1995; China 120 to 56,911 32 to >200 >300 Wu et al. 1997; Shen et al., 1993; Cheng & Liu, 1996, Ren et al., 2002 Ahmad at al., 1995; 1997; Hussain et al., Pakistan 25 to 205 >720 19 to 105 5 to 36 2014; Faheem et al., 2013
Forrester at al., 1993; Gunning and Easton, Australia >1000 >92 >40 Up to 163 1994: Gunning et al., 1996, 1998 12 ICAC RECORDER
In many countries, Helicoverpa armigera attained the status during the late vegetative phase of the cotton crop can of a major pest, replacing the traditional cotton pests, pink cause synchrony of moths and a subsequent outbreak bollworm and the tobacco caterpillar Spodoptera litura, mainly (Kranthi and Kranthi, 2010). after introduction of the synthetic pyrethroids. Synthetic pyrethroids are supposed to have suppressed populations Prolonged Absence of Outbreaks of Spodoptera litura, pink bollworm and spotted bollworm, Over the past few years, cotton pest management stabilized due but caused upsurges of H. armigera and the whitefly. The to the introduction of biotech Bt-cotton and novel eco-friendly changes in pest dynamics were mostly due to the high levels insecticides. As a result there have been hardly any reports of of pyrethroid toxicity to the pink bollworm and also on natural outbreaks from any part of the world, including countries that enemies of H. armigera and the whitefly Bemisia tabaci. did not adopt biotech Bt-cotton. Apart from the introduction Several reviews listed out the major parasitoids and predators Bt-cotton, chemicals such as spinosad, indoxacarb, emamectin of Africa that affected H. armigera in India (Romeis and benzoate, chlofenapyr, chlorantraniliprole, flubendiamide, Shannower, 1996), Africa (Youm et al., 2005) and Australia novaluron and lufenuron ensured effective control of H. (Johnson et al., 2000; Gregg and Sorocco, 2000). Van armigera. Some of the new insecticides were relatively less den Berg (1993) showed that Pheidole ants caused high toxic to predators and parasitoids in the cotton ecosystem. mortality of H. armigera in Kenya. In India, Pakistan and Over the past 15-16 years, H. armigera populations were found many other countries the egg larval parasitoid Microchilonus to be on the decline in most parts of the world. Clearly this is a curvimaculatus and larval parasitoid Campoletis were regular result of some of the following important interventions. mortality-causing factors in larvae collected from cotton • Introduction of Bt-cotton contributed to effective fields. Some of the important naturally occurring parasitoids bollworm control on H. armigera are Trichogramma chilonis (Ishii), Chelonus curvimaculatus (Cameron), Campoletis chloridae (Uchida), • Decline in the use of synthetic pyrethroids and insecticide Palexorista laxa (Curran), Eucarcelia illota (C.) and mixtures Goniopthalmus halli (Mesnil). Some major predators include • Introduction of some very useful eco-friendly molecules Geocoris ochropterus (Fabricius), Coranus spiniscutis belonging to different chemical groups such as spinosyns, (Reuter), Chrysoperla carnea (Stephens), Orius spp., Polistes avermectins, pyrroles, chitin synthesis inhibitors, spp., Chilomenes sexmaculatus (Fabricius) and spiders oxadiazines and diamides which are effective in (Oxyopes spp., Clubiona spp and Thomisus spp.). controlling H. armigera Causes of Outbreaks • Weather conditions and a combination of the above strategies The following causes are generally attributed for outbreaks of H. armigera: Management Strategies • Disruption of ecosystems: Synthetic pyrethroids and Recently, sucking pests such as leaf hoppers, thrips and insecticide mixtures have broad spectrum activity and are whiteflies have developed resistance against recommended extremely toxic to some key parasitoids and predators, insecticides. The cotton bollworm H. armigera is adapting notably the Orius spp., which were known to predate on to Bt-cotton and the pink bollworm has already developed at least 60-90% of bollworm eggs. Helicoverpa armigera high levels of resistance to Bt-cotton in India (Kranthi, 2015). was subjected to intensive and extensive chemical If unattended to, cotton pest management could revert back applications across the globe, which ironically resulted in into the uncertain phase, reminiscent of the earlier years. The outbreaks due to strong disruption of naturally occurring following set of pest management strategies are based on biological control. It was also observed (Kranthi and general principles of IPM and can be adapted to many cotton Kranthi, 2010) that avoidance of insecticides for the growing countries. first three months helps in build-up of entomophage populations such as Chrysoperla, Campoletis chloridae, Short season cotton Microchilonis curvimaculatus and Tachinids, which Short duration varieties enter into flowering phase earlier and contribute to the management of H. armigera. escape bollworm attacks during squaring-flowering stage. A narrow flowering and fruiting window in short season • Insect resistance to insecticides: Compared to its cotton, especially in early-sown crops helps the crop to predators and parasitoids, Helicoverpa armigera escape bollworm infestation by creating a mismatch between developed resistance much faster to gain the upper hand the insect-seasonal-cycles and the vulnerable reproductive in the cotton ecosystem thereby leading to frequent phase of the crop. The varieties get adequate soil moisture outbreaks. Implementation of insecticide resistance during the critical flowering and fruiting phase and give rise management strategies, is essential to keep this pest to higher yields. A shorter season of 150-160 days makes it under check, especially during years of outbreak. easier for nutrient and pest management. Adequate nutrients • Weather factors: Prolonged drought followed by rainfall such as N, P and K applied in a balanced manner, especially JUNE 2017 13 during flowering and early boll formation stage keep the and predators that keep insect pests under check. crop healthy. It is important to strictly avoid excessive Cultivation of legume intercrops should be preferred nitrogenous fertilizers and foliar application of systemic wherever possible. Crops such as soybean, clusterbean, insecticides such as organophosphates and neonicotinoids cowpea or blackgram, help in proliferation of a wide during peak vegetative phase and just prior to squaring-phase range of generalist predators and parasitoids of insect which could lead to delayed flowering, staggered flowering, pests. Borders (2-3 rows) of pigeonpea or bajra or maize prolonged vegetative phase and delayed harvest, especially in or sorghum around cotton fields was found to reduce combination with irrigation. infestation of sap sucking insects such as whiteflies, mealy bugs etc. Such crops also serve as refuge in Bt-cotton Conserve naturally occurring biological control fields forHelicoverpa armigera. These recommendations Naturally occurring biological control can be most effective are easier to implement in small scale farming systems. in pest management if the predators and parasitoids are left undisturbed to the greatest possible extent. There are several Specific strategies for bollworm management generalist predators and parasitoids that thrive in the cotton Integrated pest management (IPM), biotech cotton and eco-systems to control a wide range of insects such as the Insecticide resistante management (IRM) strategies together sucking pests and bollworms. Most of these natural enemies can play a crucial role in controlling pest populations and of insect pests are highly susceptible to insecticides and get also in delaying insect resistance development to Bt-cotton easily killed with several insecticides at low dose applications. and insecticides. IPM strategies comprising of tools to It takes a long time for the natural enemy populations to revive conserve naturally occurring biological control coupled with again, to be effective enough for biological control of major ecologically compatible tools such as botanical insecticides, insect pests. mainly neem based pesticides, biological control with There are three major strategies to protect the naturally endophytic fungi, Trichogramma spp., HaNPV (Helicoverpa occurring biological control in the cotton ecosystem. armigera Nuclear Polyhedrosis Virus), pheromone traps, light traps etc., can help in ecologically sound pest management • Cultivate varieties that are resistant to sap-sucking and mitigating insect resistance to insecticides and Bt-cotton. insects so that early season insecticide use can be avoided. Insecticide resistance management can be effective with Insecticide seed treatment will reduce the infestation careful choice and regulated use of insecticides by alternating levels of sucking pests, especially in resistant varieties. or rotating chemical groups selectively according to the • Avoid application of chemical insecticides early in the presence of pest-predator-parasitoid ratios at a specific crop- season. In the early stages of the crop, beneficial insects stage, only when necessary at economic thresholds of insect such as ladybird grubs and beetles, Chrysoperla spp., pests, after exhausting options of biological pesticides or syrphid flies,Geocoris spp., Aenasius spp., Aphilinus spp., botanical pesticides. When used within the ambit of IPM, Bt- predatory mirid bugs and spiders start getting established cotton can strengthen IPM and IRM by reducing the need for in the ecosystem. Several minor lepidopteran insects chemical insecticides. such as leaf folders, semiloopers, leaf eating caterpillars Primarily, resistance management principles are based and hairy caterpillars occur during the peak vegetative on use of a rational and sensible sequence or rotation of phase of the crop. It is important to understand that such insecticides that are effective on the target species, cause less insects are easier to control with many eco-friendly disturbance to beneficial fauna, minimize selection pressure botanical and biological pesticides. They generally do not and have unrelated resistance mechanisms or modes of cause significant damage and occur as one or two short action. The sequence of insecticides suggested under IRM cycles in the season. If the crop is not subjected to broad has been developed based on the resistance risk assessment, spectrum chemical insecticides, these minor lepidopteran pest control efficacy, ecological selectivity (based on insect pests serve as excellent hosts for parasitoids such International organization of biological control, IOBC rating) as Trichogramma spp., Apanteles spp. and Sysiropa and environmental risk assessment (based on environmental formosa, that attack H. armigera and other bollworms. impact quotient, EIQ rating) (Russell and Kranthi, 2006). Several insecticides cause a resurgence of insect pests When implemented on a large scale, the strategies were found when applied repeatedly, or indiscriminately or used to reduce insecticide resistance levels; stabilize eco-systems in mixtures. As far as possible, ecofriendly pesticides so as to encourage entomophage insect populations; reduce must be preferred especially as early season sprays, if pest populations and improve socio-economic conditions necessary at economic threshold levels of sucking pests of farmers. In general, the most successful integrated pest or bollworms, since most of them are relatively less toxic management practices are the ones that support the role of to parasitoids and predators. naturally occurring predators and parasitoids, instead of • Ecosystem engineering of crops (Bender et al., 2016): relying in the application of inoculative or inundative releases. A few crops when grown together in the same ecosystem The choice of insecticides plays a crucial role in IPM and IRM. work in tandem to favour naturally occurring parasitoids Insecticides categorized by the World Health Organization 14 ICAC RECORDER
(WHO) as Class-I (Extremely Harzardous category), such as The report also stated that the pest caused losses worth US$ phosphamidon, methyl parathion, phorate, monocrotophos, 636 million despite insecticide usage worth US$ 22 million. dichlorvos, carbofuran, methomyl, triazophos and metasystox Government of India announced a financial compensation of and all insecticide-mixtures must be avoided. Application of US$ 97 million to farmers. Whiteflies also caused serious crop synthetic pyrethroids must be avoided during the first 3-4 losses in Pakistan. months after sowing and insecticide mixtures must be avoided During the 2015-16 cotton season, a severe epidemic of all through the crop phase to prevent whitefly and other pest whitefly incidence was noticed in the cotton growing zone of outbreaks. Synthetic pyrethroids may be used only late in north India and Pakistan, beginning early August. Whitefly the season as one or at the most two sprays for the control infestation levels and cotton leaf curl virus (CLCuV) disease in of pink bollworm. Research publications show that a few July-August were higher than the previous three years in both relatively recent insecticides belonging to spinosyns, amides, countries. Whitefly infestation and the CLCuV disease were avermectins, pyrroles, chitin synthesis inhibitors, oxadiazines first noticed in early June in all the three states of north India. and diamides are compatible with IPM. A combination of late sowing of susceptible hybrids coupled Recent Exciting Research Advances with favourable weather factors for whitefly development and multiplication were the probable factors for outbreak (Singh Efficient resistance management holds the key for sustainable et al., 2016). Deficient rainfall of less than 100 mm upto pest management. In an interesting study, Ives et al. July in the cotton growing areas in the region is believed to (2017) addressed the effects of spatio-temporal variation have led to severe incidence of white fly during June and July in a management setting for two bollworm pests of cotton, thereby escalating leaf curl virus disease (Kranthi, 2015). Late Helicoverpa armigera and H. punctigera, and field data on sown crop suffered the most. In India and Pakistan, increased landscape crop distributions from Australia. They showed that whitefly infestation levels were related to high temperatures even a small proportion of Bt fields available to egg-laying above 300 C, sparse rainfall, drier spells in the monsoon and females when refuges are sparse may result in high exposure high humidity in the range of 80-90%. Indiscriminate use of to Bt for just a single generation per year and cause a surge insecticides, especially excessive pyrethroids and increased in selection. Therefore, rapid resistance evolution can occur use of nitrogenous fertilizers were also associated with when Bt crops are rare rather than common in the landscape. resurgence of the whitefly. Whitefly incidence ranged from The authors suggest that their results highlight the need to 1.6 to 90 adults /3 leaves during July-August. By the end understand spatio-temporal fluctuations in the landscape of September severe damage was caused to cotton. Fields composition of Bt crops and non-Bt habitats in order to design sprayed repeatedly with insecticides, insecticide mixtures effective resistance magement strategies. Wei et al. (2017) and pyrethroids had the highest levels of whitefly infestation showed that four laboratory strains of H. armigera with (Rishi Kumar, CICR personal communication). high levels of resistance to Cry1Ac or Cry2Ab had no cross- resistance to Vip3Aa protein thereby enabling the deployment The whitefly is a small insect of 1.0 mm in length witha of all the three toxins for sustainable management of H. waxy coating over its wings. Insecticides are less effective armigera. Wei et al. (2015) conducted studies to understand because of the waxy coating. Whiteflies cause significant cross-resistance of H. armigera for Cry1Ac and Cry2Ab. damage to crops through direct feeding, induction of host They selected H. armigera with Cry1Ac for 125 generations plant phytotoxic disorders, transmission of viruses and to produce 1000-fold resistance to Cry1Ac and 6.8-fold excretion of honeydew leading to fungal growths (Inbar and cross-resistance to Cry2Ab. Selection with Cry2Ab for 29 generations caused 5.6-fold resistance to Cry2Ab and 61-fold cross-resistance to Cry1Ac. Without exposure to Bt proteins, resistance to both proteins decreased. Results showed minor cross-resistance to Cry2Ab caused by selection with Cry1Ac and synergism between the two proteins against resistant insects suggesting that plants producing both proteins could prolong the efficacy ofBt cotton. The Whitefly Menace During the 2015-16 cropping season, a massive whitefly outbreak caused up to 50-60% crop loss in north India (Singh et al., 2016) and Pakistan. A press report in the Times of India 8th October 2015, claimed “whitefly destroys 2/3rd of Punjab’s cotton crop, 15 farmers commit suicide” http://timesofindia.indiatimes.com/india/Whitefly-destroys- 2/3rd-of-Punjabs-cotton-crop-15-farmers-commit-suicide/ Fig. 3 Whiteflies Bemisia tabaci feeding on co�on leaf articleshow/49265083.cms JUNE 2017 15
Gerling, 2008). Whiteflies suck sap from the under-surface of (De Barro et al., 2011, Cuthbertson and Vanninen, 2015). leaves causes yellowing and distortion in leaf shape causing The whitefly Bemisia tabaci is now considered as a cryptic upward curling mostly. Whiteflies excrete honey dew which species complex that is comprised of at least eleven well causes stickiness in the fibre thereby reducing the quality and defined genetic groups and at least 34 morpho-cryptic commercial value of the fibre. Whiteflies cause sticky cotton species, which are indistinguishable morphologically but fibre especially during late season infestation. The honey can be differentiated at the molecular level (De Barro et dew also attracts a fungal sooty mould and spoils leaves and al., 2011, Powell and Cuthbertson, 2013. Lee et al., 2013, bolls. The black sooty mould blocks photosynthesis in leaves Boykin and De Barro, 2014). Until recently, populations of to reduce yield. Though, the ideal conditions for growth are Bemisia tabaci were grouped into biotypes based on their 27oC and 71% relative humidity, hot and humid conditions biochemical polymorphism and biological characteristics, favour the insect. In recent times, hot and dry conditions also such as insecticide-resistance, ‘vector competence for disease favoured survival and multiplication in India. Outbreaks in transmission, vulnerability to predators and parasitoids, host India and Pakistan after 1984 were a result of weather factors range, invasiveness etc. (Brown et al., 1995; Perring, 2001; aggravated by indiscriminate use of insecticides. De Barrow et al., 2005; Xu et al., 2010). Reports also suggest The whitefly is scientifically known as Bemisia tabaci. It was that a few biotypes were characterized by the presence of first reported in Greece 125 years ago and subsequently spread certain bacterial endo-symbionts (Gottlieb et al., 2006; Chiel all across the globe. A total number of 1556 whitefly species et al., 2007) one of which conferred resistance to insecticides are documented in 161 genera (Martin and Mound, 2007). (Kontsedalov et al., 2008). These biotypes were distinguished Amongst these, Bemisia tabaci is the most damaging with by clear esterase profiles (Brownet et al., 1992; 1995). The an ability to infest more than 1000 plant species (Abd-Rabou two most invasive and damaging Bemisia tabaci biotypes are et al., 2010) and transmit more than 300 plant pathogenic B and Q. The B biotype was first identified in the late 1980s viruses (Navas-Castillo et al., 2011). Bemisia tabaci feeds on (Costa and Brown, 1991) and the Q biotype was presumed to more than 600 plant species (Quintela et al., 2016) including a have originated in the Iberian Peninsula (Guirao et al., 1997). wide spectrum of hosts such as vegetables, pulses, floriculture, Though debatable, in 1994, a new aggressive biotype ‘B horticultural crops and most notably cotton and citrus. Losses biotype’ was separated into a new species Bemisia argentifolii to cotton crop were estimated to be in the range of 15-60% and subsequently based on the mitochondrial DNA CO-1 and more under severe infestation levels. Whiteflies transmit markers, the B biotype was rechristened as Middle East- a range of viral diseases in plants. B. tabaci is the vector of Asia Minor 1 (MEAM1) species, while the Q biotype was several genera of plant viruses, of which the most widespread re-designated as the Mediterranean species (Cuthbertson and damaging are those in the genus Begomovirus (family, and Vanninen, 2015). Subsequently, biotype-specific Geminiviridae) (Quintela et al., 2016). B. tabaci transmits mitochondrial cytochrome oxidase-1 (CO1) based DNA Cotton leaf curl virus (CLCuV) to cause the dreaded cotton bar-coding methods were developed to distinguish different leaf curl disease (CLCuD) in north India and Pakistan. biotypes (Shatters et al., 2009). Recently, Hadjistylli et al., (2016) characterized the global diversity of Bemisia tabaci The taxonomy of the whitefly traversed through complex sibling species group using microsatellite markers to compare debates to further get complicated and categorized into a with species profiles derived from mitochondrial markers. complexity of cryptic species. Recent studies regrouped Their results with microsatellite markers were in broad Bemisia tabaci into a complex of 34 morphometric species agreement with the published data of mitochondrial markers. Studies conducted in Pakistan using cytochrome oxidase-1 (CO-1) with Bemisia tabaci populations collected in Pakistan indicated the presence of 15 deeply divergent lineages, including 12 from the Indo-Pakistan region comprising of six species, Asia II 1, Asia II 5, Asia II 7, Asia 1, MEAM 1, and a new species “Pakistan” (Ashfaq et al., 2014). The species Asia II 7 was not collected on cotton crop in Pakistan. Studies conducted in India using CO-1 showed the presence of five species, Asia I, Asia II-1, Asia II-7, Asia II-8, and Asia II-11 on cotton (Ellango et al., 2015). The following factors were found to have contributed to the whitefly outbreak in 2015 (Kranthi 2015): • Hot and humid conditions at early stage of the crop • Approval of varieties and hybrids that were susceptible to CLCuD and whiteflies Close-up of a whitefly. Two eggs can be seen of the stem. Photograph: Dr Vishlesh Nagrare, ICAR-CICR Nagpur, India • Late sowing 16 ICAC RECORDER
• Excess urea & irrigation at early stage of the crop developed in India. The varieties and traits if harnessed • Indiscriminate use of insecticides and mixtures properly, present good prospects for a long term solution to the whitefly-virus problem. • Whitefly resistance to insecticides • Other host crops and weeds Tolerant Varieties A few Bt-cotton hybrids and non-Bt varieties/hybrids from the • Improper spray application methods public sector were identified to be tolerant to whiteflies and • Non-compliance of ecologically consonant pest the leaf curl virus in India and Pakistan. Based on intensive management strategies screening, at least five Gossypium hirsutum genotypes, NIBGE-207, NIBGE-115, NN-3, VH-289, and MNH-886 Management Strategies were considered to be CLCuD-resistant (Abbas et al., 2015). Global experimental data (Naranjo et al., 2015) affirm that The following CLCuD tolerant varieties were identified in majority of insecticides disrupt naturally occurring biological India: LH 1556, RS 875, Maru Vikas, RS 810, HHH 223, RS control of whiteflies thereby leading to whitefly outbreaks 2013, F 1861, H 1226, CSHH 243, LH 2076, H 1236, H1098- in cotton across the world. Therefore it is important to be as improved, H 1300, RG 542 and MR 786. The following diligent as possible when insecticide recommendations are varieties were found to be tolerant to whiteflies: Supriya, made to ensure that the chemicals have as much selective Aravinda, G.Cot.Hy MDH-11 (GSGDH-2), NDLHH-240, toxicity to whiteflies without disrupting naturally occurring NDLH 1938 (Sri Rama) and MR 786. Interestingly, MR 786 biological control. In brief, indiscriminate use of insecticides, was found to be tolerant to both whitefly and the leaf curl especially chemicals with broad spectrum toxicity such as virus. organophosphates, pyrethroids, neonicotinoids and mixtures must be avoided. Excessive nitrogenous fertilizers must be Short duration varieties avoided. Use Nitrogen (N), Phosphorus (P) and Potash (P) as Early maturing short season varieties escape whiteflies mixed fertilizers in split doses based on soil testing results to especially when sown early or in time. Additionally, ensure balanced nutrition to the crop. Yellow sticky traps may termination of cotton crop in time before the onset of winter be used at 500 traps per hectare. For best long term results, facilitates timely sowing of wheat in the cotton-wheat rotation neem-oil and castor oil based insecticides, soap sprays and system of India and Pakistan. insect growth regulators are recommended. Initially vacuum suction traps may be used followed by a sequential use of Timely sowing water sprays, soap sprays and neem-oil based neem seed When compared to late sown crop, cotton sown in April or kernel extracts. If needed insect growth regulators such as before mid-May was found to be significantly more tolerant to difenthiauron, buprofezin, spiromesifen, and pyriproxifen can whiteflies and the leaf curl virus (Singhet al., 2016; Ghazanfar be used during the peak vegetative and early boll formation et al., 2007). Therefore timely sowing is an important factor in stage of the crop at recommended economic thresholds of the managing the whiteflies and the virus. whitefly. These insecticides are effective on whiteflies and are Balanced nutrient management less disruptive to predators and parasitoids of the whitefly. Following are a set of whitefly management strategies derived Application of N (nitrogen), P (phosphorus) and K (potassium) from published experimental results and are applicable more in a balanced ratio based on soil analysis to ensure adequate N for India and Pakistan. with appropriate P and K assist the crop to combat whiteflies and CLCuD. Knowledge about K nutrition on association Pest monitoring and IPM between plants and pests may help in developing strategies Whitefly management depends on proper sampling and to set up high yielding production system by reducing disease subsequent decision support systems that involve proper incidence (Zafar and Athar, 2013). Excessive nitrogen selection of pest management tools in consonance with application during vegetative phase of the crop makes the ecology of the crop to keep the pest under check with least crop vulnerable to sap-sucking insects (Bharati et al., 2012, disturbance to the ecosystem. Anusha et al., 2017) and warrants insecticide usage, which may disrupt ecological balance to cause insecticide-induced Gossypium arboreum resurgence of whiteflies. The native diploid cotton species Gossypium arboreum is cultivated in India and Paksitan. It is a potential source of Ecological balance genes for resistance to whiteflies, cotton leaf curl virus and Three species of Aphelinid parasites, Encarsia lutea (Masi), other insect pests and diseases (Vij et al., 2016). Several G. Encarsia sophia (giarualt & Dodd) and Eretmocerus mundus arboreum varieties are known to be tolerant to the whiteflies (Mercet) and predators such as Chrysopa spp., Geocoris and highly resistant (almost immune) to the Gemini virus spp., Coccinellid spp., Orius spp. and spiders were found CLCuD. Recently long staple G. arboreum varieties with to be important in naturally occurring biological control 32mm fiber length with good strength and micronaire, were of the whitefly in Pakistan (Naveed et al., 2008). At least JUNE 2017 17 three whitefly predators, Serangium parcesetosum (Sicard), insecticide mixtures must be avoided during the initial phase Cheilomenes sexmaculata (Fabricius) and Brumoides of whitefly infestation because of the possible resurgence of suturalis (Fabricius) were most commonly in cotton whiteflies when used indiscriminately (Jeyakumar and Gupta ecosystems in addition to Coccinella septempunctata 2007) (Linnaeus)., Chrysoperla zastrowi sillemi (Esben-Petersen) in north India (Kedar et al., 2014). The parasiotid Encarsia lutea Recent Exciting Research Advances (Masi) and Eretmocerus spp., were also found to be important Recent promising results with endophytic entomopathogenic components of biological control of whiteflies in north India. fungi have opened up new avenues in integrated pest Naturally occuring Aphelinid parasitoids, Encarsia formosa management. The work of Cuthbertson, (2013) and Islam et al. (Gahan) and Eretmocerus mundus (Mercet) and predators (2014) demonstrated the practical value of entomopathigenic such as Chrysoperla carnea (Stephens) and Chilomenes fungi in controlling whiteflies. They identified effective sexmaculatus (Fabricius) were observed to reduce the pest fungal species such as Isaria fumosorosea, Isaria farinosa, populations. Naturally occurring biological control in the Metarhizium anisopliae, Lecanicillium muscarium, Beauveria field is reported to have been effective to the extent of 65.0%. bassiana and Verticillium lecanii. Garrido-Jurado et al. Therefore care must be exercised to ensure that the natural (2016) showed that foliar applications of myco-insecticide ecosystems are not disrupted with inappropriate choice and strains Beauveria bassiana and Metarhizium brunneum indiscriminate use of insecticides. lead to transient endophytic colonization of crop tissues and whiteflies were infected with entomopathogenic fungi via Clean cultivation ingestion of hyphae growing as endophytes. They also showed Whiteflies have a wide host range that includes weeds on that secondary metabolites produced by the endophytic fungi which they can survive all through the year. Therefore it is contributed to the control of whitefly pests. The research opens important to keep fields and the vicinity free of weeds to the up new avenues for testing different entomopathogenic fungi best possible extent. for endophytic properties and efficacy for whitefly control. Yellow sticky traps and vacuum suction traps Genome sequencing studies have enabled the identification Yellow sticky traps (Murugan and Uthamasamy, 2001, of several useful gene sequences that can serve as a Bantewad and Thakare, 2017) were found to be useful in reference for resolving the B. tabaci cryptic species reducing pest populations. Yellow sticky traps and vacuum complex, understanding fundamental biological novelties, suction traps may be encouraged during the early phase of and providing valuable genetic information to assist the infestation. development of novel strategies for controlling whiteflies and the viruses they transmit. Chen et al. (2016) reported a Botanicals 615-Mb high-quality genome sequence of B. tabaci Middle Application of Neem oil, castor oil, cotton seed oil, fish oil rosin East-Asia Minor 1 (MEAM1), comprising of 15,664 protein- soap etc., are very effective in keeping the pest populations coding genes. The genome comprised of other expanded gene under check in the initial stage of whitefly infestation (Puri et families, including cathepsins, large clusters of tandemly al., 1998). duplicated B. tabaci-specific genes, and phosphatidyl- ethanolamine-binding proteins (PEBPs), which were found Entomopathogenic fungus to be associated with virus acquisition and transmission and/ More than 20 species of entomopathogenic fungi are or insecticide resistance, and possibly contributing to the recorded to cause whitefly mortality (Lacey et al., 1996; global invasiveness and efficient virus transmission capacity Steenberg and Humber, 1999). The most effective amongst of the species. In a novel approach, microsatellite markers these were Isaria fumosorosea, Isaria farinosa, Metarhizium were used to study genetic diversity to compare results with anisopliae, Lecanicillium muscarium, Beauveria bassiana mitochondrial DNA taxonomy. Hadjistylli et al. (2016) used and Verticillium lecanii (Cuthbertson, 2013; Islam et al., nuclear data from variable microsatellite markers to explore 2014) which caused 70 to 100% mortality in lab, green house global population structures of B. tabaci representing most and field conditions (Batta, 2003; Faria and Wraight, 2001; of the available diversity, including known monophagous, Liu and Stansly, 2000; Zaki, 1998; Quesada-Moraga et al. polyphagous, invasive, and indigenous haplotypes. The 2006). The use of entomopathogenic endophytic fungus must study showed that the invasive B and Q biotypes exhibited be explored further and ecouraged. moderate to high levels of genetic diversity, suggesting that they stemmed from large founding populations that have Insecticides maintained ancestral variation, despite homogenizing effects, For effective management of whitefly, selective insect growth possibly due to human-mediated among-population gene flow. regulating (IGR) chemicals such as buprofezin and pyriproxifen The study with its application of microsatellite markers in the should be preferred (Naranjo and Ellsworth, 2009) because characterization of global diversity, adds a new dimension to they are less toxic to natural enemies of whiteflies. Excessive the existing mitochondrial DNA markers that could be used to and indiscriminate use of synthetic pyrethroids and all kinds of unravel the cryptic diversity of the species. 18 ICAC RECORDER
Several new sources of genes were explored and a few salicylic acid concentration was low and when the whiteflies most effective genes were identified to be deployed for the were viruliferous. Exogenous salicylic acid increased the development of biotech cotton. Javaid et al. (2016) developed number and quantity of plant volatiles, especially the quantity biotech tobacco (Nicotiana tabacum) as a model system using of methyl salicylate and δ–limonene (Shi et al., 2016) phloem-specific promoters isolated from Banana bunchy top virus (BBTV) for the expression of two insecticidal proteins Cotton Leaf Curl Virus, Disease derived from Hadronyche versuta (Blue Mountains funnel- (CLCuV and CLCuD) web spider) neurotoxin (Hvt) and onion leaf lectin. They demonstrated that transgenic plants expressing Hvt alone Cotton leaf curl virus (CLCuV) is a major pathogen in India or in combination with onion leaf lectin were resistant to and Pakistan and is a threat to China and several other cotton Phenacoccus solenopsis (cotton mealybug), Myzus persicae growing countries. The Cotton leaf curl disease (CLCuD) has (green peach aphids) and Bemisia tabaci (silver leaf whitefly). been causing severe economic losses in the indo-Pak region The expression of both proteins under different phloem- intermittently in epidemic cycles over the past twenty years. specific promoters resulted in close to 100% mortality and Unfortunately, there is no cure for the ailment after it strikes. provided robust protection. Raza et al. (2016) showed that The best method to combat the disease is to develop resistant osmoregulation of feeding in whiteflies could be disrupted varieties. Managing the insect vector whitefly, Bemisia through RNA interference in biotech tobacco plants by tabaci may partly reduce the intensity of disease. Scientific expressing double stranded RNA (dsRNA) to silence efforts in India and Pakistan over the recent past have been aquaporin (AQP) and a sucrase gene and alpha glucosidase commendable. The disease can be effectively mitigated with (AGLU) which are involved in maintaining osmotic pressure combined efforts of the two countries. in whiteflies. More than 70% mortality was observed in Cotton leaf curl viral disease (CLCuD) is transmitted by Bemisia tabaci after six days of feeding on plants expressing viruliferous whitefly, Bemisia tabaci. The B-biotype, now re- dsRNA. The study clearly demonstrated that downregulation designated as Middle Easy Asia Minor -1 (MEAM1) is known of genes related to osmoregulation may find practical as the most viruliferous. The whitefly takes about 30 minutes applications for the control of whiteflies on cotton. Shukla for virus-acquisition and 10 minutes for transmission. The et al. (2016) developed biotech cotton plants expressing a virus complex infects plant cells and multiplies using the cell protein (Tma12) from an edible fern, Tectaria macrodonta DNA for its survival and replication. Inter-cellular movement (Fee) that was insecticidal to whitefly. Results of contained occurs through the plasmodesmata to spread in cells and other field trials showed that the biotech cotton lines expressing plant parts of the plant. Typically the symptoms in leaves Tma12 at ~0.01% of total soluble leaf protein were resistant start with vein thickening followed by leaf thickening, finally to whitefly infestation and the whitefly transmitted cotton leaf resulting in deformed cup shaped curled leaf, sometimes curl disease with no detectable yield penalty. with enations as outgrowth from the midrib of the lower leaf In an important discovery of genes mediating cotton host plant surface. In severe cases of infection, the virus causes complete resistance to whiteflies, Li et al. (2016) used transcriptome distortion of plant parts and stunting, thereby resulting in total studies to identify WRKY40 and copper transport protein as yield losses. hub genes that are likely to regulate cotton defenses to whitefly CLCuD outbreaks were first reported from Nigeria in 1912 infestation. Silencing of G. hirsutum mitogen activated protein and 1924 and subsequently in 1926 from Tanzania. The kinase-3 (GhMPK3) by virus-induced gene silencing (VIGS) disease caused persistent problems for several years in resulted in suppression of the jasmonic acid and ethylene various parts of Africa. During the 1950s, the disease caused pathways leading to enhanced whitefly susceptibility, thereby estimated losses of 30-40% in Gezira, Sudan. Though the suggesting that the candidate insect resistant genes identified Egyptian cotton species Gossypium barbadense is most in the study are credible and offer significant utility. susceptible, the disease incidence has been at low levels in Exogenous application of botanically derived repellents and Egypt. Reports of leaf curl virus in Guangdong and Guangxi natural products to induce host plant resistance to whiteflies provinces of China (Cai et al., 2010) indicate the worrying were also found to be promising. Geraniol and citronellol were possibility of long range accidental spread, which could not found to be most effective repellents against Bemisia tabaci rule out the possibility of the disease invading the main cotton (Deletre et al. 2016). The authors also found that 1.0% (w/w growing regions of central and south India. In the Indo-pak or v/v) of the essential oils from lemongrass (Cymbopogon region, CLCuD was first noticed in 1967 near Multan in citratus), cinnamon (Cinnamomum zeylanicum), cumin Pakistan (Hussain and Ali, 1975), but turned into an epidemic (Cuminum cyminum) and citronella (Cymbopogon in Multan only in 1988. The introduction and cultivation of winternarius) caused 96.3% mortality for cinnamon oil, the highly susceptible varieties S12 and CIM-70 in 1988 is 64.7% for citronella oil, 61.0% for lemongrass oil and 30.0% presumed to have triggered the infection into an epidemic for cumin oil after 4 hours of exposure. Exogenous application form. The area under S12 reached about 46% area in Punjab- of salicylic acid caused plants to repel non-viruliferous B and Pakistan (Briddon and Markham, 2000) and the disease started Q biotype whiteflies, but the effect was reduced when the gaining hold. Symptoms were noticed from 1973 onwards in JUNE 2017 19 popular cotton varieties such as 149-F and B-557. More and the cotton leaf curl Burewala virus (CLCuBuV) have been more new hairy varieties that were tolerant to leaf hoppers but most damaging. The first epidemic was caused by the Multan susceptible to whiteflies were replacing the glabrous (smooth virus in 1998 and the subsequent epidemics after 2002 in leaf) varieties that were susceptible to leaf hoppers but were India and Pakistan were dominated by the Burewala virus. tolerant to whiteflies. The change effectively replaced leaf Both the species operate through a monopartite Begomovirus hoppers with whiteflies in the cotton eco-system of Pakistan. complex that is comprised of a circular single stranded DNA The disease gradually spread over Multan, Khanewal and (ssDNA) molecule supported by two smaller circular non- Vehari to reach an epidemic level in 1993 to an area of viral single stranded DNA molecules called alpha-satellite 0.89 million hectares that accounted for about one-third of and beta-satellite. The two molecules play a crucial role for Pakistan’s total cotton area. Losses due to CLCuD ‘Multan disease expression. They suppress the host defense systems epidemic’ (Zhou et al., 1998) were estimated to be 30-40% to enhance virulence thus accelerating the disease. The beta at a production of 1.34 million tons in an epidemic year in satellite CLCuMuB plays a role in disease transmission 1994-95 as compared to 2.17 million tons in 1991-92. Yield through replication, systemic movement in plants and by losses to the extent of 80.0% were being recorded. The disease trans-encapsidation in the helper virus’ coat protein. The alpha caused an estimated loss of US$ 5.0 Billion in five years from satellite replicates independently. It also enables a continuous 1992 to 1997 (Briddon and Markham, 2000). virus transmission by the whitefly vector by sustaining the The, Indo-Pak region is known to have the following six presence of the CLCuBuV and the beta-satellite in the host species of Begomoviruses that may occur individually plants for a longer time. or in combination in infected plants. 1. Cotton leaf curl The Multan epidemic was found to have been caused by three Burewala virus (CLCuBuV), 2. Cotton leaf curl Alabad virus species of Begomoviruses, namely Cotton leaf curl Alabad (CLCuAlV), 3. Cotton leaf curl Kokhran virus (CLCuKoV), virus (CLCuAlV), Cotton leaf curl Kokhran virus (CLCuKoV), 4. Cotton leaf curl Multan virus (CLCuMuV), 5. Cotton leaf and CLCuMuV (Zhou et al., 1998) which were associated curl Rajasthan virus (CLCuRaV) and 6. Papaya leaf curl virus with a single species of betasatellite Cotton leaf curl Multan (PaLCuV). Additionally the tomato leaf curl Bangalore virus betasatellite (CLCuMuB) and satellite-like component Cotton (ToLCBaV) which was reported to be present in southern leaf curl Multan alphasatellite (CLCuMuA). Subsequent India is an impending threat for cotton and is a possible source reports showed that Tomato leaf curl Bangalore virus for the evolution of new highly virulent recombinant viruses. (ToLCBaV) and Papaya leaf curl virus (PaLCuV) were also The CLCuD in Pakistan is caused by a complex of five single- infecting cotton (Mansoor et al., 2003; Kirthi et al., 2004). stranded DNA viruses belonging to genus Begomovirus Plant breeders responded quickly to identify CLCuD tolerant (family Geminiviridae) along with their DNA satellites, viz. varieties to stabilize cotton production for about 10 years. betasatellite and alphasatellite (Brown et al., 2015). CLCuD The Indian variety LRA 5166 developed by ICAR-CICR was in the Indo-Pak region is caused mainly by single stranded widely used as a resistant donor in India and Pakistan to develop monopartite DNA Begomoviruses (genus Begomovirus: new varieties that could withstand the virus. With sustained family, Geminiviridae) that are encapsulated in twin quasi- efforts, the disease declined until the year 2000, with only icosahedral capsid geminate particles. Thus far two major sporadic instances of infection. However, a new strain named species, the cotton leaf curl Multan virus (CLCuMuV) and as Cotton leaf curl Burewala virus (CLCuBuV) appeared in 2001-02 season in the Punjab province of Pakistan and caused the ‘Burewala epidemic’ by infecting all cotton varieties of Pakistan. Cotton production was reduced to 1.7 million tons in the years 2002 and 2003. The new ‘Burewala CLCuBuV species’ had infected all the varieties that were resistant to the ‘Multan CLCuMuV species’. (Amrao et al., 2010; Sattar et al., 2013). The Burewala strain was supposed to have formed from the recombination of two virulent species of Pakistan called ‘Multan species’ and Kokhran species’. Further, a new strain named CLCuMuBBur evolved from the recombination of CLCuMuB and Tomato leaf curl betasatellite (Amin et al., 2006). Recently, two new strains were identified from the Sindh province of Pakistan. One of them was the African strain Cotton leaf curl Gezira virus (CLCuGeV) and the other was Shahdadpur virus (CLCuShV) (Amrao et al., 2010; Tahir et al., 2011). The origins of the most damaging virus strains have so far been traced to CLCuKoV and CLCuMuV. The presence Co�on leaves damaged due to CLCuV. of new strains such as the African CLCuGeV (Cotton Leaf Photograph: Dr D. Monga, ICAR-CICR, Nagpur (Regional Sta�on, Sirsa) , India Curl Gezira Virus) and the Shahdadpur virus (CLCuShV) 20 ICAC RECORDER pose a new threat for possibilities of not only direct damage Clearly the efforts paid off and damage due to CLCuD but also for the possible evolution of new recombinant viruses declined significantly in India during the years 1998 to 2006 that can play havoc in virulence. due to the cultivation of resistant varieties, extensive weed While so far, bipartite begomo viruses were reported only management and implementation of stringent IPM measures from Africa, and CLCuD in Indo-Pak region was caused by to manage whiteflies and the leaf curl virus. However, the mono-partite viruses, recently bipartite Begomoviruses such complete replacement of public sector varieties with new as the Tomato leaf curl virus (ToLCV) (Zaidi et al., 2015) Bt cotton hybrids/varieties by the private companies after and Tomato leaf curl New Delhi virus (ToLCNDV) were also 2007 changed the scenario completely in India and Pakistan. reported from cotton plants over a vast area in Punjab in CLCuD started showing up in again in north India due to Pakistan. Concerns were enhanced with the synergistic action the progressive replacement of the CLCuD tolerant varieties of ToLCNDV in enhancing the infection of Burewala virus with commercial Bt-cotton hybrids. Staring from 2009 within (Zaidi et al., 2016). 3-4 years, the disease established itself firmly in almost all the main cotton growing districts of Punjab and Haryana In India CLCuD was first noticed in 1989 in Sriganganagar with high levels of severity in Ferozepur, Muktsar, Faridkot, district of Rajasthan along the Pakistan border (Ajmera,1994) Abohar and Fazilka, Jind, Fatehabad, Hisar and Sirsa districts. and on G. barbadense at Indian Agricultural Research The disease intensity was less severe in Rajasthan because, Institute, New Delhi in 1989 (Anonymous, 1990; Varma et unlike Punjab and Haryana, Rajasthan did not adopt the new al., 1993). Over the subsequent few years, CLCuD spread to Bt cotton hybrids so readily. Bt cotton hybrid area in Punjab the cotton growing districts in north Indian states to assume and Haryana reached 70% by 2008, whereas in Rajasthan serious proportions of almost an epidemic form in 1996 only 25% of the area in 2008 was under Bt-cotton hybrids. and 1997 affecting 0.2 million hectares, especially in north Data suggest that indiscriminate introduction and cultivation Rajasthan and adjoining regions of Punjab and Haryana. The of new hybrids could have been one of the major factors in disease soon spread to the interior cotton growing regions of creating congenial conditions for the CLCuD in north India. Haryana and Punjab in north India (Rishi and Chauhan,1994) and established itself as a major problem in cotton production Causes for CLCuD Epidemics in in north India. Surprisingly, India experienced the leaf curl India and Pakistan virus outbreaks in 1993 and 1996 just concurrent to the A combination of factors such as long duration bushy hybrids, occurrence of epidemics in Pakistan during 1992 and 1995 susceptibility to whiteflies and CLCuD, late sowing, excessive (Kranthi 2015a). A new virus called Cotton leaf curl Rajasthan application of nitrogenous fertilizers and indiscriminate use virus (CLCuRV) that evolved from recombination of Multan of insecticides and insecticide mixtures with broad spectrum (CLCuMV) & Kokhran (CLCuKV) viruses, was reported action caused frequent outbreaks of whiteflies and the leaf to occur in Rajasthan (Malathi et al. 2004). Until 2003, the curl disease in India. ‘Multan CLCuMuV’ and the ‘Rajasthan CLCuRaV’ were the main species that caused the CLCuD in India, after which Following are some of the main causal factors for outbreaks: the ‘Burewala CLCuBuV’ virus replaced the two viruses • Late sown crop is more vulnerable to whiteflies and and became the main dominant species. The Burewala strain CLCuD. Bt-cotton hybrids sown late showed significantly could infect all the varieties that were resistant to other strains higher disease at all locations in north India (Monga, of the virus, mainly the ‘Multan species’. Recent studies by 2016). Similar observation were recorded in Pakistan and Rajagopalan et al., (2012), showed that CLCuD in north other countries (Iqbal et al., 2008; Iqbal and Khan., 2010; India was mainly caused by the cotton leaf curl Burewala Tanveer and Mirza, 1996; James et al., 2004). virus (CLCuBuV) and three of its variants which displaced • Increase in nitrogenous fertilizers to harness hybrid CLCuRV and CLCuKoV isolates. However, CLCuD in Delhi vigour. Excessive canopy provided congenial micro- was found to be caused by CLCuRV (Rajasthan), CLCuMuV climate for sucking pests and whiteflies to thrive. (Multan), and Burewala CLCuBuV species (Godara et al., 2015; 2017). • The mandatory requirement of varietal tolerance to CLCuD was diluted in India for the private sector Bt- In India, for about 15-16 years after 1990, the cotton research cotton hybrids during the period 2007 to 2013. Thus a net-work and the varietal approval committees in India had large number of varieties & hybrids that were susceptible made it mandatory that only varieties or hybrids resistant to to CLCuD and the whiteflies were approved, which led the CLCuD would be approved for identification, notification to rapid spread of the disease across north India and and cultivation in north India. Plant breeding and evaluation Pakistan. Seed-cotton yields were reduced by 15.7% to efforts were intensified through the All India Coordinated 56.7% (Monga, 2014). Cotton Improvement Program (AICCIP). Several resistant varieties such as RST9, RS875, RS810, RS2013, F1861, • Majority of the commercial hybrids were susceptible to LH2076, H117, H1126 and resistant hybrids LHH144, sap-sucking insects. Indiscriminate use of insecticides CSH198, CSHH238 and CSHH243 were developed and and insecticide mixtures during the early vegetative stage cultivated until 2007 to combat the disease effectively. of the crop to control sucking pests disrupted naturally JUNE 2017 21
occurring biological control, thereby causing resurgence al., 1998; Farooq et al., 2011; Briddon and Markham, 2000). of whiteflies. Clean cultivation should be practised. Off-season weeds • Excessive use of insecticides with broad spectrum must be destroyed and clean cultivation should be followed toxicity aggravated whitefly infestation. scrupulously during the season to minimize sources of virus inoculums. Several weed species were found to harbour and Management Strategies sustain the ‘Burewala species’ inoculum all across north The most important management strategies are related to India. Notable amongst these are Althea rosea, Achyranthus early sowing of CLCuD-tolerant varieties. balanced nutrition aspera, Chenopodium album, Convolvulus arvensis, Croton by avoiding excessive nitrogenous ferilizers and conserving sperciflorus, Clerodeadron eneansi, Corchorus acutangularis, naturally occurring biological control by diligent selection and Eclipta alba, Parthenium hysterophorus, Lantana camara, use of selective eco-friendly insecticides to manage whitefly Sida spinosa, Trianthema monogyna and Tribulus terrestris. populations. The following strategies were recommended in Monitoring and management both India and Pakistan, based on research results from the Regular pest and disease monitoring and initiation of two countries. appropriate IPM measures based on economic thresholds, Timely or early sowing are important steps for effective management of whiteflies Government efforts should be streamlined to ensure that canal and the virus. The whitefly species Bemisia tabaci in North water is released in time to avoid late sowing. Late sown crop India has been recently showing high level of resistance to the creates congenial conditions for the disease to get aggravated recommended insecticides, thus enhancing insect survival and and thus creates more viral and whitefly inoculum in the farm thereby increased transmission of virus. ecosystems. Early sowing must be encouraged to provide Recent Exciting Research Advances conditions for the crop to escape pest and disease infestation. Commendable efforts were made in India and Pakistan to Tolerant varieties identify gene resources to be deployed for the development of Regulatory authorities should enforce a strict ban on the biotech cotton varieties that can withstand the virus. Biotech approval of varieties and hybrids that are susceptible to cotton expressing a double stranded RNA-insert homologous CLCuD in India and Pakistan, to ensure that only tolerant/ to the intergenic region (IR) of Cotton leaf curl Rajasthan virus resistant genotypes are approved, released and cultivated. (CLCuRV) was developed using an intron hairpin (ihp) RNAi Plant breeders must identify resistant sources of germplasm construct. Transformed cotton plants showed the presence of lines on priority and attempts must be made to pyramid siRNAs and upon inoculation with viruliferous whiteflies, resistance genes. CLCuD resistant varieties such as FH- none of the nine plants with independent events displayed 682, CIM-240, CRIS-9, BH-36, CIM-109 and CIM-1100 in any CLCuD symptoms even after 90 days post inoculation Pakistan and RST9, RS875, RS810, RS2013, F1861, LH2076, (Khatoon et al., 2016). Sohrab et al. (2016) developed biotech H117, H1126 in India must be used as sources of resistance to cotton plants by using βC1 gene in antisense orientation gene be used in breeding programmes to develop new varieties that to control CLCuD. Molecular studies confirmed a single can tolerate Burewala virus. copy integration in the genome. The plants were tested in green house and open field conditions and were found to Native desi species confer resistance through reduced infection and delayed Cultivation of the native diploid species Gossypium arboreum symptom appearance. Iqbal et al. (2016) proposed a broad and Gossypium herbaceum must be promoted, especially in spectrum CLCuD controlling method based on multiplexed the districts bordering India and Pakistan. The two species are clustered regulatory interspaced short palindromic repeats almost immune to all the species of leaf curl viruses. CRISPR/Cas9 system where a cassette of synthetic guide RNA (sgRNA) is designed to target not only the whole Reducing the load of virus inoculum in CLCuD-associated Begomovirus complex but also the the crop environment associated satellite molecules. They devised a multiplex Infected plants must be destroyed after harvest. Crop rotation sgRNA cassette targeting IR and replication-associated plans must be devised with alternate crops that are not protein (Rep) of the CLCuD-associated Begomoviruses host plants for whiteflies. Cultivation of American cotton, (CABs), non-coding intergenic regions (IR) of Cotton leafcurl Gossypium hirsutum must be avoided in orchards and near Burewala virus associated with recombinant Cotton leaf curl malvaceous crops such as okra (bhendi) or tomato especially Multan betasatellite (CLCuMuB) and rep gene of diverse in disease prone areas. Simultaneous cultivation of cotton alphasatellites. This system offers a flexible approach for with alternate hosts such as vegetable and citrus intensifies stacking multiple nucleases as one transgene, thereby offering the disease inoculum. It was observed that whitefly picks targeted cleavage of mixed infections by multiple viruses and virus from egg plant, okra, Ablemoschus esculentus and associated DNA-satellites, such as CLCuD-complex. Hibiscus rosa-sinensis and primary sites of infection are Interesting studies were conducted to unravel the association formed in cotton plants (Gusain et al., 1991; Muhammad et and interactions between whiteflies, viruses and plants. Wang 22 ICAC RECORDER et al. (2016) reported a gene from the MEAM-1 (B biotype) Bt-cotton technology which in combination with the existing Bemisia tabaci BtPGRP, encoding a PGRP that binds and ‘bollworm-controlling’ Bt-cotton technologies and the boll kills bacteria in vitro. Begomovirus infection led to increased weevil eradication program could herald a new beginning expression of BtPGRP. The authors detected in vitro for sustainable pest management in South America. The interaction between BtPGRP and TYLCV and recorded the whiteflies and leaf curl viruses are significant threats to cotton co-localization of TYLCV and BtPGRP in whitefly mid-gut. in Pakistan and north India. Researchers in both countries The study addresses a visible gap in understanding whitefly found that the best way to combat both problems was through immunity and provides insight into how the whitefly immunity four simple strategies. 1. Early sowing, 2. Varieties tolerant to acts in complex mechanisms of Begomovirus transmission CLCuD, 3. Balanced NPK nutrition, and 4. Diligent choice of among plants. Peptidoglycan recognition proteins (PGRPs) insecticides. Non-adherence to any of the four strategies could are multifunctional pattern recognition proteins. Further, result in serious problems with the pest and disease. Biotech Shalev et al. (2016) idenfied a knottin gene, knot-1 which cotton technologies were developed for resistance to whiteflies was found to play a role in restricting the quantity of virions and the CLCuD in India and Pakistan. Collaborative efforts an insect may acquire and transmit. The authors suggest that between the two countries to pyramid the new biotech events knot-1 protects B. tabaci against deleterious effects caused by into elite varieties for resistance to the two problems can TYLCV by limiting the amount of virus associated with the tackle the menace in a sustainable manner. The problem of Bt- whitefly vector. In a path breaking study, the phenomenon of resistant pink bollworm is serious, but manageable. Scientists ‘autophagy’ was reported in cotton plants (Haxim et al., 2017) in the US showed how a combination of three technologies 1. as a novel anti-pathogenic mechanism that plays an important Bt-cotton 2. Gossyplure pheromones for mass trapping and role in antiviral immunity in plants. The authors reported that mating disruption and 3. Mass release of biotech-male sterile the cotton plant autophagic machinery mainly comprising moths, could effectively diminish the problem. Additionally of the key autophagy protein ATG8 targets the virulence proper compliance of refuge strategy strengthened the ‘pink factor βC1 of Cotton leaf curl Multan virus (CLCuMuV) to bollworm eradication’ program. There is a lot to learn from degrade it, thus conferring resistance in plants. Haxim et al. the technological and administrative essence of the success (2017) also showed that a V32A mutation in βC1 abolished stories to combat the problems efficiently. its interaction with NbATG8f, and virus carrying βC1V32A References showed increased symptoms and viral DNA accumulation Abbas, A., Iqbal, M.A., Rahman, M.U. and Paterson, A.H., 2015. in plants. Furthermore, silencing of autophagy-related Estimating genetic diversity among selected cotton genotypes and genes ATG5 and ATG7 reduced plant resistance to the DNA the identification of DNA markers associated with resistance to viruses CLCuMuV. The study opens up a new scope for the cotton leaf curl disease. Turkish Journal of Botany, 39 (6):1033- exploration of autophagy genes, which must be identified 1041. and used to develop biotech plants for enhanced resistance Abbas, G., M. Farhan, I. Haq and G. Ghouse, 2016. Accelerating to viruses. infestation of pink bollworm Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae) on Bt–varieties of cotton in Pakistan. Conclusion Pak. Entomol., 38(2):109-113. The four insect pests, bollweevil, pink bollworm, cotton Abd-Rabou, S, Simmons, A.M., 2010. Survey of reproductive bollworm and whitefly are global pests. The whitefly and host plants of Bemisia tabaci (Hemiptera: Aleyrodidae) in Egypt, pink bollworms are prevalent everywhere in the world. The including new host records. Entomol News, 121:456–65. boll weevil is currently restricted to the Western Hemisphere. Agarwal, R.A., Katiyar, K.N., 1979. An estimate of losses of seed The cotton bollworm was confined so far to Africa, Asia, kapas and seed due to bollworms on cotton in India. Indian Journal Europe and Australasia. But the recent discovery of the cotton of Entomology, 41(2):143-148 bollworm Helicoverpa armigera in South America signals Aguiar, R.W.S., Martins, E.S., Ribeiro, B.M. and Monnerat, R.G. new agri-concerns for the continent. The leaf curl virus disease (2012) Cry10Aa protein is highly toxic to Anthonomus grandis is limited to Pakistan and north India. These problems are Boheman (Coleoptera: Curculionidae), an important insect pest in serious. They have been causing enormous economic losses Brazilian cotton crop fields.Bt Res. 3, 20–28 to cotton in various parts of the world. Through commendable Ahmad, M., Arif, I.M. and Ahmad, Z., 1995. Monitoring insecticide efforts, the boll weevil problem was managed scientifically resistance of Helicoverpa armigera (Lepidoptera: Noctuidae) in in the US through a ‘bollweevil eradication program’ Pakistan. Journal of Economic Entomology, 88(4), pp.771-776. and recently in Mexico with the help of the United States Ahmad, M., Arif, M.I. and Attique, M.R., 1997. Pyrethroid Department of Agriculture (USDA). The recent discovery of resistance of Helicoverpa armigera (Lepidoptera: Noctuidae) in H. armigera in Brazil, Argentina, Uruguay and Paraguay and Pakistan. Bulletin of entomological research, 87(04), pp.343-347. the damaging presence of boll weevils in these countries in Ahmad, M., Iqbal Arif, M. and Ahmad, Z., 1999. Patterns of resistance South America are worrisome. The two pests not only cause to organophosphate insecticides in field populations of Helicoverpa crop losses but also lead to progressive increase in the use armigera in Pakistan. Pesticide science, 55(6), pp.626-632. of insecticide applications. In an impressive development, Ahmad, N., Ashraf, M., Fatima, B., 2001. Integration of mating researchers in Brazil have claimed to have made a new biotech JUNE 2017 23 disruption technique and parasitoids for the management of cotton Barbosa, L.D.F., Yuki, V.A., Marubayashi, J.M., De Marchi, B.R., bollworms. Pakistan Journal of Zoology, 33(1):57-60. Perini, F.L., Pavan, M.A., de Barros, D.R., Ghanim, M., Moriones, Ajmera, B.D., 1994. Occurrence of leaf curl virus on American E., Navas-Castillo, J. and Krause-Sakate, R., 2015. First report of Cotton (G. hirsutum) in North Rajasthan. Poster presentation, Bemisia tabaci Mediterranean (Q biotype) species in Brazil. Pest National Seminar on Cotton Production Challenges in 21st Century, Management Science, 71(4): 501-504. April 18-20, Hisar, India. Barbosa, S. And Ramos, G. A., 2014. High input cotton production: Akhtar, Z.R., M.J. Arif, Mansoor-ul-Hassan, B. Sadia, U. Irshad, benefits and consequences – the case of Brazil. https://www.icac.org/ M. Majid and Y.G. Yin, 2016. Genetic resistance in pink bollworms getattachment/mtgs/Plenary/73rd-Plenary/Agenda/OS6-Barbosa.pdf against transgenic cotton: an evidence from Pakistan. Pak. Entomol., Batta, Y.A., 2003. Production and testing of novel formulations of the 38(2):153-157 entomopathogenic fungus Metarhizium anisopliae (Metschinkoff) Alemandri, V., De Barro, P., Bejerman, N., Caro, E.A., Dumon, A.D., Sorokin (Deuteromycotina: Hyphomycetes). Crop Protection, 22(2), Mattio, M.F., Rodriguez, S.M. and Truol, G., 2012. Species within the pp.415-422. Bemisia tabaci (Hemiptera: Aleyrodidae) complex in soybean and Beasley, C.A., Adams, C.J., 1995. Effects of irrigation, irrigation bean crops in Argentina. Journal of Economic Entomology, 105(1): timing, and cotton boll burial on extent and patterns of pink bollworm 48-53. spring emergence. Southwestern Entomologist, 20(1):73-106 Amin, I., Mansoor, S., Amrao, L., Hussain, M., Irum, S., Zafar, Y., et Behere, G.T., Tay, W.T., Russell, D.A., Heckel, D.G., Appleton, al. 2006. Mobilisation into cotton and spread of a recombinant cotton B.R., Kranthi, K.R. and Batterham, P., 2007. Mitochondrial DNA leaf curl disease satellite. Arch. Virol. 151, 2055–2065. doi: 10.1007/ analysis of field populations of Helicoverpa armigera (Lepidoptera: s00705-006-0773-4 Noctuidae) and of its relationship to H. zea. BMC evolutionary Amrao, L., Akhtar, S., Tahir, M.N., Amin, I., Briddon, R.W. and biology, 7(1), p.117. Mansoor, S.. 2010. Cotton leaf curl disease in Sindh province of Bender, S.F., Wagg, C. and van der Heijden, M.G., 2016. An Pakistan is associated with recombinant begomovirus components. underground revolution: biodiversity and soil ecological engineering Virus Res 153:161-65. for agricultural sustainability. Trends in ecology & evolution, 31(6), Amrao, L., Amin, I., Shahid, M.S., Briddon, R.W. and Mansoor, S., pp.440-452. 2010b. Cotton leaf curl disease in resistant cotton is associated with Bharathi, S., Prasada Rao, G.M.V., Kumari, R.S., Chengareddy, V., a single begomovirus that lacks an intact transcriptional activator 2012. Influence of plant geometry and nitrogen levels on performance protein. Virus Res 152:153–63. of cotton hybrids under rainfed conditions in vertisols of Andhra Anonymous., 1990. Cotton leaf curl virus is a whitefly transmitted Pradesh. Journal of Cotton Research and Development. 26:204-206 geminivirus. Annual Report, IARI, New Delhi. Bink, F.A., 1975. Leaf curl and mosaic diseases of cotton in central Anusha, S., Rao, G.P. and Kumar, D.S.R., 2017. Influence of different Africa. Cotton Growers Rev 52: 133- 41. nitrogen levels on the management of Bt cotton sucking pests. Boykin, L.M. and De Barro, P.J., 2014. A practical guide to Araújo, C.L., Bezerra, I.W., Oliveira, A.S., Moura, F.T., Macedo, identifying members of the Bemisia tabaci species complex: and L.L., Gomes, C.E., Barbosa, A.E., Macedo, F.P., Souza, T.M., other morphologically identical species. Frontiers in Ecology and Franco, O.L. and Bloch-J, C., 2005. In vivo bioinsecticidal activity Evolution, 2, p.45. toward Ceratitis capitata (fruit fly) and Callosobruchus maculatus Briddon, R.W., and Markham, P.G., 2000. Cotton leaf curl virus (cowpea weevil) and in vitro bioinsecticidal activity toward different disease. Virus Research 71: 151-59. orders of insect pests of a trypsin inhibitor purified from tamarind Brown, J.K., Coats, S.A., Bedford, I.D., Markham, P.G., Bird, J., tree (Tamarindus indica) seeds. Journal of agricultural and food Frohlich, D.R., 1995. Characterization and distribution of esterase chemistry, 53(11), pp.4381-4387. electromorphs in the whitefly, Bemisia tabaci (Genn.) (Homoptera: Armes, N.J., Jadhav, D.R. and DeSouza, K.R., 1996. A survey Aleyrodidae). Biochem. Genet. 33:205–14 of insecticide resistance in Helicoverpa armigera in the Indian Brown, J.K., Coats, S.A., Bedford, I.D., Markham, P.G., Bird, J., subcontinent. Bulletin of entomological research, 86(05), pp.499- 1992. Biotypic characterization of Bemisia tabaci populations based 514. on esterase profiles, DNA fingerprinting, virus transmission, and Arnemann, J.A., James, W.J., Walsh, T.K., Guedes, J.V.C., Smagghe, bioassay to key host plant species. Phytopathology, 82:1104 G., Castiglioni, E. and Tay, W.T., 2016. Mitochondrial DNA COI Brown, J.K., Frohlich, D.R. and Rosell, R.C., 1995. The sweetpotato characterization of Helicoverpa armigera (Lepidoptera: Noctuidae) or silverleaf whiteflies: biotypes of Bemisia tabaci or a species from Paraguay and Uruguay. Genet Mol Res, 15(2). complex?. Annual review of entomology, 40(1), pp.511-534. Ashfaq, M., Hebert, P.D., Mirza, M.S., Khan, A.M., Mansoor, S., Brown, J.K., Perring, T.M., Cooper, A.D., Bedford, I.D. and Markham, Shah, G.S. and Zafar, Y., 2014. DNA barcoding of Bemisia tabaci P.G., 2000. Genetic analysis of Bemisia (Hemiptera: Aleyrodidae) complex (Hemiptera: Aleyrodidae) reveals southerly expansion of populations by isoelectric focusing electrophoresis. Biochemical the dominant whitefly species on cotton in Pakistan. PloS one, 9(8), genetics, 38(1), pp.13-25. p.e104485. Brown, J.K., Zerbini, F.M., Navas-Castillo, J., Moriones, E., Bantewad, S.D. and Thakare, A.Y., 2017. Evaluation of colour Ramos-Sobrinho, R., Silva, J.C., Fiallo-Olivé, E., Briddon, sticky traps at various heights for monitoring of whitefly Bemesia R.W., Hernández-Zepeda, C., Idris, A. and Malathi, V.G., 2015. tabaci (Gennadius) in cotton. Journal of Cotton Research and Revision of Begomovirus taxonomy based on pairwise sequence Development, 31(1):116-122 comparisons. Archives of Virology, 160(6), pp.1593-1619. 24 ICAC RECORDER
Cai, J.H., Xie, K., Lin, L., Qin, B.X., Chen, B.S., Meng, J.R. and formulation of gossyplure. Indian Journal of Agricultural Sciences, Liu, Y.L., 2010. Cotton leaf curl Multan virus newly reported 63(3):193-194 to be associated with cotton leaf curl disease in China. Plant Dhurua, S. and Gujar, G.T., 2011. Field-evolved resistance to Bt pathology, 59(4), pp.794-795. toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella Carriere, Y., Ellers-Kirk, C., Kumar, K., Heuberger, S., Whitlow, (Saunders)(Lepidoptera: Gelechiidae), from India. Pest management M., Antilla, L., Dennehy, T.J. and Tabashnik, B.E., 2005. Long-term science, 67(8), pp.898-903. evaluation of compliance with refuge requirements for Bt cotton. Pest Ellango, R., Singh, S.T., Rana, V.S., Gayatri Priya, N., Raina, H., management science, 61(4): 327-330. Chaubey, R., Naveen, N.C., Mahmood, R., Ramamurthy, V.V., Cheema, M.A., Muzaffar, N., Ghani, M.A., 1980. Biology, host range Asokan, R. and Rajagopal, R., 2015. Distribution of Bemisia tabaci and incidence of parasites of Pectinophora gossypiella (Saunders) in genetic groups in India. Environmental entomology, 44(4): 1258- Pakistan. Pakistan Cottons, 24(1):37-73 1264. Chen, W., Hasegawa, D.K., Kaur, N., Kliot, A., Pinheiro, P.V., Luan, Faheem, U., Nazir, T., Saleem, M., Yasin, M. and Bakhsh, M., 2013. J., Stensmyr, M.C., Zheng, Y., Liu, W., Sun, H. and Xu, Y., 2016. The Status of insecticide resistance in Helicoverpa armigera (Hübner) in draft genome of whiteflyBemisia tabaci MEAM1, a global crop pest, southern Punjab, Pakistan. Sarhad J. Agric, 29(4): 563-572. provides novel insights into virus transmission, host adaptation, and Faria, M. and Wraight, S.P., 2001. Biological control of Bemisia insecticide resistance. BMC biology, 14(1), p.110. tabaci with fungi. Crop protection, 20(9): 767-778. Cheng, G. and Liu, Y., 1996. Cotton bollworm resistance and its Farooq, A., Farooq, J., Mahmood, A., Batool, A., Rehman, A., development in northern cotton region of China 1984–1985. Resistant Shakeel, A., Riaz, M., Shahid, M.T.H. and Mehboob, S., 2011. An Pest Management, 8(1), pp.32-33. overview of cotton leaf curl virus disease (CLCuD) a serious threat Chiel, E., Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Katzir, to cotton productivity. Australian Journal of Crop Science, 5(13), N., Inbar, M. and Ghanim, M., 2007. Biotype-dependent secondary p.1823. symbiont communities in sympatric populations of Bemisia Fitt, G.P., 1994. Cotton pest management: part 3. An Australian tabaci. Bulletin of entomological research, 97(04), pp.407-413. perspective. Annual review of entomology, 39(1), pp.543-562. Colvin, J.T., 1990. Laboratory studies on the regulation of migration Fitt, G.P., 1989. The ecology of Heliothis species in relation to of the cotton bollworm, Heliothis armigera (Hb.) (Lepidoptera: agroecosystems. Annu. Rev. Entomol. 34, 17–52. Noctiodae). PhD Thesis, University College of North Wales, Bangor Fitt, G.P., Wilson, L.J., 2000. Genetic engineering in IPM: Bt cotton, in: Costa, H.S., and Brown, J.K., 1991. Variation in biological Kennedy GG, Sutton TB (Eds.) Emerging Technologies in Integrated characteristics and esterase patterns among populations of Bemisia Pest Management: Concepts, Research and Implementation, APS tabaci (Genn.) and the association of one population with silverleaf Press, St Paul, MN, USA, pp. 108–125. symptom induction. Entomol Exp Appl. 61:211–219. Forrester, N.W., Cahill, M., Bird, L.J. and Layland, J.K., 1993. Section Cuthbertson, A.G., 2013. Update on the status of Bemisia tabaci in 8. Pyrethroid resistance: field resistance mechanisms. Bulletin of the UK and the use of entomopathogenic fungi within eradication entomological research supplement series, 1, pp.54-61. programmes. Insects, 4(2), pp.198-205. Frisbie RE., El-Zik., K.M., Wilson, L.T., 1989. The future of cotton Cuthbertson, A.G., and Vänninen, I., 2015. The importance IPM. Integrated pest management systems and cotton production of maintaining Protected Zone status against Bemisia New York, USA; John Wiley and Sons, Inc., 413-428 tabaci. Insects, 6(2): 432-441. Gao, Z.R., Zhao, H.Y. and Jiang, Y.F., 1992. A study on the occurrence, Czepak, C., Albernaz, C., Vivan, L. M., Guimarães, H. O. & damage and control of the pink bollworm in Henan Province. Plant Carvalhais, T. 2013. First reported occurrence of Helicoverpa Protection, 18(4), pp.29-30. armigera (Hübner) (Lepidoptera: Noctuidae) in Brazil. Pesq. Agropec. Trop., Goiânia 43, 110–113. Garrido-Jurado, I., Resquín-Romero, G., Amarilla, S.P., Ríos- Moreno, A., Carrasco, L. and Quesada-Moraga, E., 2016. Transient Darling, H.S., 1951. Pink bollworm, Platyedra gossypiella endophytic colonization of melon plants by entomopathogenic fungi (Saund.), as a pest of cotton at Zeidab, northern Sudan. Bulletin of after foliar application for the control of Bemisia tabaci Gennadius Entomological Research, 42:157-167 (Hemiptera: Aleyrodidae). Journal of Pest Science, pp.1-12. De Barro, P.J., Liu, S.S., Boykin, L.M. and Dinsdale, A.B., 2011. Ghazanfar, M.U., Sahi, S.T., Ilyas, M.B. and Randhawa, M.A., Bemisia tabaci: a statement of species status. Annual review of 2007. Influence of sowing dates on CLCuV incidence in some cotton entomology, 56, pp.1-19. varieties. Pakistan Journal of Phytopathalogy, 19, pp.177-180. De Barro, P.J., Trueman, J.W.H. and Frohlich, D.R., 2005. Bemisia Godara, S., Khurana, S.P. and Biswas, K.K., 2017. Three variants argentifolii is a race of B. tabaci (Hemiptera: Aleyrodidae): the of cotton leaf curl begomoviruses with their satellite molecules molecular genetic differentiation of B. tabaci populations around the are associated with cotton leaf curl disease aggravation in New world. Bulletin of entomological research, 95(03), pp.193-203. Delhi. Journal of Plant Biochemistry and Biotechnology, 26(1), Deletre, E., Chandre, F., Barkman, B., Menut, C. and Martin, T., pp.97-105. 2016. Naturally occurring bioactive compounds from four repellent Godara, S., Saini, N., Khurana, S.P. and Biswas, K.K., 2015. Lack essential oils against Bemisia tabaci whiteflies. Pest management of resistance in cotton against cotton leaf curl begomovirus disease science, 72(1): 179-189. complex and occurrence of natural virus sequence variants. Indian Dhawan, A.K. and Simwat, G.S., 1993. Management of pink Phytopathology, 68(3), pp.326-333. bollworm (Pectinophora gossypiella) through a sprayable JUNE 2017 25
Gottlieb, Y., Ghanim, M., Chiel, E., Gerling, D., Portnoy, V., Hussain, T., Ali, M., 1975. A review of cotton diseases in Pakistan. Steinberg, S., Tzuri, G., Horowitz, A.R., Belausov, E., Mozes-Daube, Pak Cottons 19: 71-86. N. and Kontsedalov, S., 2006. Identification and localization of a Inbar, M. and Gerling, D., 2008. Plant-mediated interactions between Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Applied whiteflies, herbivores, and natural enemies. Annu. Rev. Entomol. 53, and Environmental Microbiology, 72(5), pp.3646-3652. 431–448. Gowda, C.L.L., 2005. Helicoverpa- The global problem. In Sharma, Ingram, W.R., 1994. Pectinophora (Lepidoptera: Gelechiidae), in H. C. Ed. Heliothis/ Helicoverpa management: Emerging trends and Insect Pests of Cotton, ed. by Matthews GA and Tunstall JP. CAB strategies for future research. 2005. Oxford and IBH Publishing Co, International, Wallingford, UK, pp. 107–149. New Delhi (469 pages). Iqbal, M. and Khan, M.A., 2010. Management of Cotton leaf curl Gregg, P.C. and Del Socorro, A.P., 2000. Techniques used to virus by planting time and plant spacing. Adv Agri Botanics (2)1. determine the mating behaviour of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in relation to host plants. Austral Iqbal, M., 1993. Detection, transmission and control of cotton leaf Entomology, 39(3), pp.188-194. curl virus. M.Sc Thesis, Deptt Agri Ent Univ Agric., Faisalabad, p55. Guirao, P., Beitia, F., and Cenis, J.L., 1997. Biotype determination Iqbal, M., Khan, N,I., Hayat, K. and Muhammad, T., 2008. of Spanish populations of Bemisia tabaci (Hemiptera: Aleyrodidae). Management of cotton crop under high Cotton Leaf Curl Virus Bull Entomol Res. 87:587–593. attack. Asian J Plant Sci 6: 1125-30. Gunning, R.V. and Easton, C.S., 1994. Endosulfan resistance Iqbal, Z., Sattar, M.N. and Shafiq, M., 2016. CRISPR/Cas9: A tool in Helicoverpa armigera (Hübner)(Lepidoptera: Noctuidae) in to circumscribe cotton leaf curl disease. Frontiers in plant science, 7. Australia. Austral Entomology, 33(1): 9-12. Islam, M.T., Omar, D. and Shabanimofrad, M., 2014. Molecular Gunning, R.V., Moores, G.D. and Devonshire, A.L., 1996. Insensitive identification and virulence of six isolates of Metarhizium Acetylcholinesterase and Resistance to Thiodicarb in Australian anisopliae (Deuteromycotina: Hyphomycetes) to Bemisia tabaci Q Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Pesticide biotype. Journal of Asia-Pacific Entomology, 17(3), pp.237-241. Biochemistry and Physiology, 55(1): 21-28. Ives, A.R., Paull, C., Hulthen, A., Downes, S., Andow, D.A., Gunning, R.V., Moores, G.D. and Devonshire, A.L., 1998. Insensitive Haygood, R., Zalucki, M.P. and Schellhorn, N.A., 2017. Spatio- Acetylcholinesterase and Resistance to Organophosphates in Temporal Variation in Landscape Composition May Speed Resistance Australian Helicoverpa armigera. Pesticide Biochemistry and Evolution of Pests to Bt Crops. PloS one, 12(1), p.e0169167. Physiology, 62(3):147-151. Jackson, C.G., Neemann, E.G. and Patana, R., 1979. Parasitization Gunning, R.V., Moores, G.D. and Devonshire, A.L., 1998. Insensitive of 6 lepidopteran cotton pests by Chelonus blackburni [Hym.: acetylcholinesterase causes resistance to organophosphates Braconidae]. Biocontrol, 24(1): 99-105. in Australian Helicoverpa armigera (Hübner)(Lepidoptera: James, J.M., Wright, D.L., Wiatrak, P.J. and Vargas, M.A. 2004. Noctuidae). Pest Management Science, 54(3), pp.319-320. Effect of row width and nitrogen on cotton morphology and canopy Gusain, T., Tahir, M. and Mahmood, T., 1991. Cotton Leaf Curl microclimate. Crop Sci 44: 707-10. Disease. A Review, Pak J Phytopath 3 (1-2): 57-61. Javaid, S., Amin, I., Jander, G., Mukhtar, Z., Saeed, N.A. and Hadjistylli, M., Roderick, G.K. and Brown, J.K., 2016. Global Mansoor, S., 2016. A transgenic approach to control hemipteran Population Structure of a Worldwide Pest and Virus Vector: Genetic insects by expressing insecticidal genes under phloem-specific Diversity and Population History of the Bemisia tabaci Sibling promoters. Scientific Reports, 6. Species Group. PloS one, 11(11), p.e0165105. Jeyakumar, P. and Gupta, G.P., 2007. Insecticide induced biochemical Hariton Shalev, A., Sobol, I., Ghanim, M., Liu, S.S. and Czosnek, H., changes in cotton and consequent resurgence of whitefly. Pesticide 2016. The Whitefly Bemisia tabaci Knottin-1 Gene Is Implicated in Research Journal, 19(1), pp.90-92. Regulating the Quantity of Tomato Yellow Leaf Curl Virus Ingested Jin, L., Zhang, H.N., Lu, Y.H., Yang, Y.Y., Wu, K.M., Tabashnik, and Transmitted by the Insect. Viruses, 8(7), p.205. B.E., Wu, Y.D. 2015. Large-scale test of the natural refuge strategy Haxim, Y., Ismayil, A., Jia, Q., Wang, Y., Zheng, X., Chen, T., Qian, for delaying insect resistance to transgenic Bt crops. Nat. Biotechnol., L., Liu, N., Wang, Y., Han, S. and Cheng, J., 2017. Autophagy 33, 169–174. functions as an antiviral mechanism against geminiviruses in Johnson, M.L., Pearce, S., Wade, M., Davies, A., Silberbauer, L., plants. eLife, 6, p.e23897. Gregg, P. and Zalucki, M., 2000. Review of beneficials in cotton Head, G., and Dennehy, T., 2010. Insect resistance management for farming systems. Cotton Research and Development Corporation. transgenic Bt cotton, in Cotton: Biotechnological Advances, ed. by Kedar, S.C., Saini, R.K., Kumaranag, K.M. and Sharma, S.S., Zehr, U.B., Springer, Berlin, Germany, pp. 113–125. 2014. Record of natural enemies of whitefly, Bemisia tabaci Hillocks, R.J., Minja, E., Mwaga, A., Nahdy, M.S. and (Gennadius)(Hemiptera: Aleyrodidae) in some cultivated crops in Subrahmanyam, P., 2000. Diseases and pests of pigeonpea in eastern Haryana. Journal of Biopesticides, 7(1), p.57. Africa: a review. International Journal of Pest Management, 46(1), Khatoon, S., Kumar, A., Sarin, B.N. and Khan, J.A. 2016. RNAi- pp.7-18. mediated resistance against Cotton leaf curl disease in elite Indian Hussain, D., Saleem, H.M., Saleem, M. and Abbas, M., 2014. cotton (Gossypium hirsutum) cultivar Narsimha. Virus genes 52 (4): Monitoring of insecticide resistance in field populations of 530-37. Helicoverpa armigera (Hub.)(Lepidoptera: Noctuidae). J. Entomol. King, A.B.S., 1994. Heliothis/Helicoverpa (Lepidoptera: Noctuidae). Zool. Stud, 2, pp.1-8. In: Matthews, G.A., Tunstall, J.P. (Eds.), Insect Pests of Cotton. CAB 26 ICAC RECORDER
International, UK, pp. 39-106. Macedo, L.L.P., Júnior, J.A.D.S., Coelho, R.R., Fonseca, F.C.A., Kirthi, N., Priyadarshini, C.G.P., Sharma, P., Maiya, S.P., Hemalatha, Firmino, A.A.P., Silva, M.C.M., Fragoso, R.R., Albuquerque, V., Sivaraman, P., Dhawan, Rishi, N. and Savithri, H.S. 2004. Genetic E.V.S., Silva, M.S., de Almeida Engler, J. and Terra, W.R., 2017. variability of begomoviruses associated with cotton leaf curl disease Knocking down chitin synthase 2 by RNAi is lethal to the cotton boll originating from India. Arch Virol 149: 2047–57. weevil. Biotechnology Research and Innovation. Kontsedalov, S., Zchori-Fein, E., Chiel, E., Gottlieb, Y., Inbar, M. Malathi, V.G., Padamalatha, K.V., Sivalingam, P., Gandhakrishnan, and Ghanim, M., 2008. The presence of Rickettsia is associated with N., Mandal, B., Monga, D., Ajmera, B.D., Varma, A. 2004. increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) Begomoviruses causing cotton leaf curl disease in India. In: National to insecticides. Pest Manag Sci 64:789–792. seminar on cotton leaf curl virus disease: present status and future strategies for its management at central institute for cotton research Kranthi, K.R., Jadhav, D., Wanjari, R., Kranthi, S. and Russell, D., regional station, Sirsa, Haryana 92p. 2001. Pyrethroid resistance and mechanisms of resistance in field strains of Helicoverpa armigera (Lepidoptera: Noctuidae). Journal Malik, M. F. 2001. Biological Control of Pink Bollworm of Economic Entomology, 94(1), pp.253-263. (Pectinophora gossypiella, Lepidoptera: Gelechiidae) by Trichogrammatoidea bactrae (Hymenoptera: Trichogrammatidae) Kranthi, K.R., Jadhav, D.R., Wanjari, R.R., Ali, S.S. and Russell, D., in cotton (Gossypium barbadense). J. Bio. Sci., 1(2): 56-57. 2001a. Carbamate and organophosphate resistance in cotton pests in India, 1995 to 1999. Bulletin of entomological research, 91(01), Manjanuth, T.M., Bhatnagar, V.S., Pawar, C.S., Sitanatham, S., 1989. pp.37-46. Economic importance of Heliothis spp. in India and an assessment of their natural enemies and host plants. In: King EG, Jackson RD (eds) Kranthi, K.R., Jadhav, D.R., Kranthi, S., Wanjari, R.R., Ali, S. & Proceedings of the Workshop on Biological Control of Heliothis: Russell, D., 2002. Insecticide resistance in five major insect pests of Increasing the Effectiveness of Natural Enemies November 1985, cotton in India. Crop Protection, 21: 449-460. New Delhi. New Delhi, India: Far Eastern Regional Research Office, Kranthi, K.R. and Kranthi, S. 2010. Cotton Crop Protection in the US Department of Agriculture, 196-228. 21st Century. (Ed. Phil Wakelyn & Rafiq Chaudhry) International Mansoor, S., Briddon, R.W., Bull, S.E., Bedford, I.D., Bashir, A., Cotton Advisory Committee publication. Pp. 99-120 Hussain, M., Saeed, M., Zafar, Y., Malik, K.A., Fauquet, C. and Kranthi, K.R., 2012. Bt cotton Q&A. 1-72. Indian Society for Cotton Markham, P.G., 2003. Cotton leaf curl disease is associated with Improvement, (ISCI). Central Institute for Research on Cotton multiple monopartite begomoviruses supported by single DNA Technology, Adenwala Road, Matunga, Mumbai, India. p. 1-72. β. Archives of virology, 148(10), pp.1969-1986. Kranthi, K.R., 2015. Pink bollworm strikes Bt cotton. Cotton Martin, J. and Mound, L., 2007. An annotated check list of Statistics News, 35: 1-6. http://www.cicr.org.in/pdf/Kranthi_art/ the world’s whiteflies (Insecta: Hemiptera: Aleyrodidae). Pinkbollworm.pdf Lista de las moscas blancas del mundo (Insecta: Hemiptera: Aleyrodidae). Zootaxa, 1(492), pp.1-84. Kranthi, K.R., 2015a. Whitefly –The Black Story. CAI Statistics and News. 23: 1-3 http://cicr.org.in/pdf/Kranthi_art/Whitefly.pdf Martin, T., Ochou, G.O., Djihinto, A., Traore, D., Togola, M., Vassal, J.M., Vaissayre, M. and Fournier, D., 2005. Controlling Kranthi, S., Satija, U., Pusadkar, P., Rishi Kumar, Shastri, C. S., an insecticide-resistant bollworm in West Africa. Agriculture, Ansari, S., Santosh, H. B., Monga, D and Kranthi, K. R. 2017. Non- ecosystems & environment, 107(4), pp.409-411. Bt seeds provided by seed companies in India – are they suitable as refuge for Bt-cotton? Current Science, 112, 1992-1993. McCaffery, A.R., 1999. Resistance to insecticides in heliothine Lepidoptera: a global view. Insecticide resistance: From mechanisms Lacey, L.A., Fransen, J.J. and Carruthers, R., 1996. Global to management, pp.59-74. distribution of a naturally occurring fungi of Bemisia, their biologies and use as biological control agents. Bemisia: 1995, taxonomy, Medel, V., Palma, R., Mercado, D., Rebolledo, R., Quiroz, biology, damage, control and management. A. and Mutis, A., 2015. The effect of protease inhibitors on digestive proteolytic activity in the Raspberry Weevil, Aegorhinus Lee, W., Park, J., Lee, G-S., Lee, S., Akimoto, S., 2013. Taxonomic superciliosus (Guerin)(coleoptera: Curculionidae). Neotropical status of the Bemisia tabaci complex (Hemiptera: Aleyrodidae) and entomology, 44(1): 77-83. reassessment of the number of its constituent species. PLoS ONE 8: e63817. Miller, J.R. and Gut, L.J., 2015. Mating disruption for the 21st century: matching technology with mechanism. Environmental Li, J., Zhu, L., Hull, J.J., Liang, S., Daniell, H., Jin, S. and Zhang, entomology, 44(3): 427-453. X., 2016. Transcriptome analysis reveals a comprehensive insect resistance response mechanism in cotton to infestation by the phloem Mironidis, G.K., Kapantaidaki, D., Bentila, M., Morou, E., feeding insect Bemisia tabaci (whitefly). Plant biotechnology Savopoulou-Soultani, M. and Vontas, J., 2013. Resurgence of the journal. cotton bollworm Helicoverpa armigera in northern Greece associated with insecticide resistance. Insect science, 20(4), pp.505-512. Liu, T.X. and Stansly, P.A., 2000. Insecticidal activity of surfactants and oils against silverleaf whitefly (Bemisia argentifolii) nymphs Mohan, K.S., Ravi, K.C., Suresh, P.J., Sumerford, D. and Head, (Homoptera: Aleyrodidae) on collards and tomato. Pest management G.P., 2015. Field resistance to the Bacillus thuringiensis protein science, 56(10), pp.861-866. Cry1Ac expressed in Bollgard® hybrid cotton in pink bollworm, Pectinophora gossypiella (Saunders), populations in India. Pest Luo, S.B., Yan, J.P., Chai, C.J., Liang, S.P., Zhang, Y.M., Zhang, Y., Management Science. Le, G.K., 1986. Control of pink bollworm, Pectinophora gossypiella with Bacillus thuringiensis in cotton fields. Chinese Journal of Monga, D., 2014. Status of cotton leaf curls virus disease in India. Biological Control, 2(4):167-169 Presented in 6th meeting of Asian Cotton Research and Development JUNE 2017 27
Network Held in Dhaka, Bangladesh from 18-20 June 2014, Full gossypiella (Lepidoptera: Gelechiidae), populations. GM crops & paper available at www.icac.org . food, 5(4), pp.280-286. Monga, D., 2015. Evaluation of Bt cotton hybrids at different Oliveira, G.R., Silva, M.C., Lucena, W.A., Nakasu, E.Y., Firmino, locations in north zone. (Personal communication). A.A., Beneventi, M.A., Souza, D.S., Gomes, J.E., de Souza, J.D., Monga, D., 2016. Cotton leaf curl virus disease: an Rigden, D.J. and Ramos, H.B., 2011. Improving Cry8Ka toxin overview. Agricultural Research Journal, 53(4), pp.466-474. activity towards the cotton boll weevil (Anthonomus grandis). BMC biotechnology, 11(1), p.85. Monga, D., Chakrabarty, P.K. and Kranthi, R., 2011. Cotton leaf Curl Disease in India-recent status and management strategies. Presented Oliveira, R.S., Oliveira-Neto, O.B., Moura, H.F., de Macedo, L.L., in 5th meeting of Asian Cotton Research and Development Network Arraes, F.B., Lucena, W.A., Lourenço-Tessutti, I.T., de Deus Barbosa, Held in Lahore in Feb. 23-25 Full paper available at www.icac.org . A.A., da Silva, M.C. and Grossi-de-Sa, M.F., 2016. Transgenic Cotton Plants Expressing Cry1Ia12 Toxin Confer Resistance to Monga, D., Kumar, R., Solanki, P. and Kayasth, M. 2015. Fall Armyworm (Spodoptera frugiperda) and Cotton Boll Weevil Management of cotton leaf curl virus disease through innovative (Anthonomus grandis). Frontiers in plant science, 7: 1-11 interventions. Cotton Res J 6: 7-12. Pedgley, D.E., 1985. Windborne migration of Heliothis armigera Morrison, N.I., Simmons, G.S., Fu, G., O’Connell, S., Walker, A.S., (Hubner) (Lepidoptera: Noctuidae) to the British Isles. Entomologist’s Dafa’alla, T., Walters, M., Claus, J., Tang, G., Jin, L. and Marubbi, Gazette, 36(1):15-20 T., 2012. Engineered repressible lethality for controlling the pink bollworm, a Lepidopteran pest of cotton. PloS one, 7(12), p.e50922. Pedgley, D.E., Tucker, M.R. and Pawar, C.S., 1987. Windborne migration of Heliothis armigera (Hübner)(Lepidoptera: Noctuidae) Mu, J. and Wang, H., 1995. The cause of violent occurence and in India. International Journal of Tropical Insect Science, 8(4-5-6): control tactic of Heliocoverpa armigera Hubner. Journal of 599-604. Shandong Agricultural University, 27, pp.1-7. Perring, T.M., 2001. The Bemisia tabaci species complex. Crop Prot Muhammad, F., Tariq, A.H., Ihsan, J. and Saleem, A., 1998. 20:725–737. Evaluation of two Cotton leaf curl virus transmission techniques and their response to different cotton cultivars. Pak J Phytopath 10:18– Phokela, A. and Mehrotra, K.N. 1989. Pyrethroid resistance in 22. Helicoverpa armigera (Hub.) II.Permeability and metabolism of cypermethrin. Proceedings of Indian National Science Academy Murúa, M.G., Scalora, F.S., Navarro, F.R., Cazado, L.E., Casmuz, B55: 235-238. A., Villagrán, M.E., Lobos, E. and Gastaminza, G., 2014. First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Phokela, A., Dhingra, S. and Mehrotra, K.N. 1989. Pyrethroid Argentina. Florida Entomologist, 97(2), pp.854-856. resistance in Heliothis armigera Hubner. Response to cypermethrin. Proceedings of the National Academy of Sciences, India, 59 (B). 373- Murugan, M. and Uthamasamy, S., 2001. Yellow sticky trap 380. monitored whitefly, Bemisia tabaci (Gennadius) population on cotton cultivars. Madras Agricultural Journal, 88(1/3): 126-127. Powell, M.E. Cuthbertson, A.G.S., 2013. Pest control Distinguishing between different biotypes of Bemisia tabaci in the UK. The Naranjo, S.E. and Ellsworth, P.C., 2009. Fifty years of the integrated Biologist, 60, 18‒21. 8. control concept: moving the model and implementation forward in Arizona. Pest management science, 65(12): 1267-1286. Puri, S.N., Murthy, K.S. and Sharma, O.P., 1998. Integrated management of cotton whitefly, Bemisia tabaci Naranjo, S.E., Ellsworth, P.C. and Frisvold, G.B., 2015. Economic (Gennadius). Ecological agriculture and sustainable development, 2; value of biological control in integrated pest management of 286-296. managed plant systems. Annual review of entomology, 60: 621-645. Quesada-Moraga, E., Maranhao, E.A.A., Valverde-García, P. Navas, L.E., Berretta, M.F., Pérez, M.P., Amadio, A.F., Ortiz, E.M., and Santiago-Álvarez, C., 2006. Selection of Beauveria bassiana Sauka, D.H., Benintende, G.B. and Zandomeni, R.O., 2014. Sequence isolates for control of the whitefliesBemisia tabaci and Trialeurodes and expression of two cry8 genes from Bacillus thuringiensis vaporariorum on the basis of their virulence, thermal requirements, INTA Fr7-4, a native strain from Argentina. Journal of molecular and toxicogenic activity. Biological control, 36(3); 274-287. microbiology and biotechnology, 24(4), pp.241-248. Quintela, E.D., Abreu, A.G., Lima, J.F.D.S., Mascarin, G.M., dos Navas-Castillo, J., Fiallo-Olive, E., Sanchez-Campos, S., 2011. Santos, J.B. and Brown, J.K., 2016. Reproduction of the whitefly Emerging virus diseases transmitted by whiteflies. Annu Rev Bemisia tabaci (Hemiptera: Aleyrodidae) B biotype in maize fields Phytopathol. 49:219–48. (Zea mays L.) in Brazil. Pest management science, 72(11), pp.2181- Naveed Muhammad., Khalid Abdullah., Muhammad Tahir Jan., 2187. Shabana Wazir. and Rabia Saeed., 2017. New Pests - New Challenges. Rabello, A.R., Queiroz, P.R., Simões, K.C., Hiragi, C.O., Lima, L.H., ICAC Recorder. Pp. 6-12 Oliveira, M.R.V. and Mehta, A., 2008. Diversity analysis of Bemisia Naveed, M., Salam, A., Saleem, M.A. and Ali H. Sayyed., 2008. tabaci biotypes: RAPD, PCR-RFLP and sequencing of the ITS1 Effect of Foliar Applications of Some Insecticides on Bemisia rDNA region. Genetics and Molecular Biology, 31(2): 585-590. tabaci, Predators and Parasitoids: Implications in Its Management in Raj, R., Sekhon, P.S. and Sangha, M.K., 2016. Protection against Pakistan. Phytoparasitica 36(4): 377-387 cotton leaf curl disease by Jasmonic acid induced proteins. J Cotton Ojha, A., Sree, K.S., Sachdev, B., Rashmi, M.A., Ravi, K.C., Res Dev 30 (1): 84-89. Suresh, P.J., Mohan, K.S. and Bhatnagar, R.K., 2014. Analysis of Rajagopalan, P.A., Naik, A., Katturi, P. and Kurulekar, M., 2012. resistance to Cry1Ac in field-collected pink bollworm, Pectinophora Dominance of resistance-breaking cotton leaf curl Burewala virus (CLCuBuV) in northwestern India Arch. Virol 157: 855-68. 28 ICAC RECORDER
Raza, A., Malik, H.J., Shafiq, M., Amin, I., Scheffler, J.A., Scheffler, Shen, J., Wu, Y., Chen, J., Zhou, W., Zhou, B., Tan, F. and You, B.E. and Mansoor, S., 2016. RNA interference based approach to Z., 1994. The basic research of resistance management in cotton down regulate osmoregulators of whitefly (Bemisia tabaci): Potential bollworm (Lepidoptera: Noctuidae). Resistant pest management technology for the control of whitefly. PloS one, 11(4), p.e0153883. (USA). Ren, X., Han, Z. and Wang, Y., 2002. Mechanisms of monocrotophos Shen, J.L., Wu, Y.D., Tan, J.G., Zhou, B.H., Chen, J. and Tan, resistance in cotton bollworm, Helicoverpa armigera F.J., 1993. Comparison of two monitoring methods for pyrethroid (Hübner). Archives of insect biochemistry and physiology, 51(3), resistance in cotton bollworm (Lepidoptera: Noctuidae). Resistant pp.103-110. pest management (USA). Ribeiro, T.P., Arraes, F.B.M., Lourenço-Tessutti, I.T., Silva, M.S., Shi, X., Chen, G., Tian, L., Peng, Z., Xie, W., Wu, Q., Wang, S., Zhou, Lisei-de-Sá, M.E., Lucena, W.A., Macedo, L.L.P., Lima, J.N., Santos X. and Zhang, Y., 2016. The Salicylic Acid-Mediated Release of Plant Amorim, R.M., Artico, S. and Alves-Ferreira, M., 2017. Transgenic Volatiles Affects the Host Choice of Bemisia tabaci. International cotton expressing Cry10Aa toxin confers high resistance to the Journal of Molecular Sciences, 17(7), p.1048. cotton boll weevil. Plant Biotechnology Journal. Shukla, A.K., Upadhyay, S.K., Mishra, M., Saurabh, S., Singh, R., Riley, J.R., Armes, N.J., Reynolds, D.R., Smith, A.D., 1992. Singh, H., Thakur, N., Rai, P., Pandey, P., Hans, A.L. and Srivastava, Nocturnal observations on the emergence and flight behaviour S., 2016. Expression of an insecticidal fern protein in cotton protects of Helicoverpa armigera (Lepidoptera: Noctuidae) in the post- against whitefly. Nature Biotechnology, 34(10), pp.1046-1051. rainy season in central India. Bulletin of Entomological Research, Silva, C.R., Monnerat, R., Lima, L.M., Martins, E.S., Melo Filho, 82(2):243-256 P.A., Pinheiro, M.P. and Santos, R.C., 2015. Stable integration and Rishi, N. and Chauhan, M.S. 1994. Appearance of leaf curl disease of expression of a cry1Ia gene conferring resistance to fall armyworm cotton in northern India. J Cotton Res Dev 8: 179-80. and boll weevil in cotton plants. Pest Manag. Sci. 11, 1–9. Romeis, J. and Shanower, T.G., 1996. Arthropod natural enemies Simmons, G.S., McKemey, A.R., Morrison, N.I., O’Connell, S., of Helicoverpa armigera (Hübner)(Lepidoptera: Noctuidae) in Tabashnik, B.E., Claus, J., Fu, G., Tang, G., Sledge, M., Walker, India. Biocontrol Science and Technology, 6(4), pp.481-508. A.S. and Phillips, C.E., 2011. Field performance of a genetically Russell, D. and Kranthi, K.R., 2006. Cotton bollworm control engineered strain of pink bollworm. PloS one, 6(9), p.e24110. in small-scale production systems handbook. Common Fund for Sims, M.A., Dennehy, T.J., Patin, A., Carrière, Y., Liu, Y.B., Commodities, Amsterdam. Tabashnik, B., Antilla, L. and Whitlow, M., 2001. Arizona’s multi- Saad, A.S.A., Tayeb, E.H.M., Awad, H.A. and ElBassiunoy, H.M. agency resistance management program for Bt cotton: sustaining the 2012. The release of the parasitoid Trichogramma evancens to susceptibility of pink bollworm, Cotton: A College of Agriculture control the pink bollworm Pectinophora gossypiella (Saunders) and Report. in Proceedings – 2001 Beltwide Cotton Conferences, 9–13 the side-effect of certain insecticides on it. Alexandria Sci. Exchange January 2001, Anaheim, California, ed. by Dugger, P. and Richter, J., 33: 1-9. D.A., National Cotton Council, Memphis, TN, pp. 1175–1179. Sabry, A. H., Hassan, K.A. and Rahman, A.A., 2014. Relative Simwat, G.S., Dhawan, A.K., Sidhu, A.S., 1988. Effect of constant toxicity of some modern insecticides against the pink bollworm, temperature and relative humidity on the termination of larval Pectinophora gossypiella (Saunders) and their residues effects on diapause in pink bollworm. Journal of Insect Science, 1(2):133-135 some natural enemies. Int. J. Sci. Environ. Tech., 3(2): 481-491 Singh, D., Singh, P., Gill, J.S. and Brar, J.S. 2010. Weather based Sattar, M.N., Kvarnheden, A., Saeed, M. and Briddon, R.W., 2013. prediction model for forcasting cotton leaf curl disease in American Cotton leaf curl disease–an emerging threat to cotton production cotton. Indian Phytopath 63 (1) : 87-90. worldwide. J Gen Virol 94(4): 695-710. Singh, J., Sandhu, S.S. and Sindhu, A.S. 1988. Adult emergence Schwartz, P.H., 1983. Losses in yield of cotton due to insects. pattern of parasitoid Apanteles angaleti and its known hosts during Agriculture Handbook, USDA, No. 589:329-358 offseason in Punjab. Biocontrol, 33(3): 309-314 Sevacherian, V. and El Zik, K.M., 1983. A slide rule for cotton crop Singh, S., Pandher, S., Rathore, P., Sharma, A., Singh, K. and and insect management. Cotton Gin and Oil Mill Press. 13 pp. Gumber R.K., 2016. From conventional to Bt cotton and bollworms to whitefly: cotton Cultivation under threat in northern india. Shalev, A.H., Sobol, I., Ghanim, M., Liu, S.S. and Czosnek, H., Beltwide Cotton Conferences, New Orleans, LA, January 5-7, 2016. 2016. The Whitefly Bemisia tabaci Knottin-1 Gene Is Implicated in PP 830-835 Regulating the Quantity of Tomato Yellow Leaf Curl Virus Ingested and Transmitted by the Insect. Viruses, 8(7), p.205. Sohrab, S.S., Kamal, M.A., Ilah, A., Husen, A., Bhattacharya, P.S. and Rana, D., 2016. Development of Cotton leaf curl virus resistant Sharma, H.C., 2001. Cotton bollworm/legume pod borer, transgenic cotton using antisense ßC1 gene. Saudi journal of Helicoverpa armigera (Hubner)(Noctuidae: Lepidoptera): biology biological sciences, 23(3), pp.358-362. and management. Crop protection compendium, 72. Sosa-Gómez et al. 2015. Timeline and geographical distribution Shatters, R.G., Powell, C.A., Boykin, L., Liansheng, H., McKenzie, of Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae: C.L., 2009. Improved DNA barcoding method for Bemisia tabaci and Heliothinae) in Brazil. Revista Brasileira de Entomologia 60, 101– related Aleyrodidae: Development of universal and Bemisia tabaci 104 biotype-specific mitochondrial cytochrome c oxidase I polymerase chain reaction primers. J. Econ. Entomol. 2009, 102, 750–758 Steenberg, T. and Humber, R.A., 1999. Entomopathogenic Potential of Verticillium and Acremonium Species (Deuteromycotina: Shen, J. and Wu, Y., 1995. Resistance of Helicoverpa armigera to Hyphomycetes). Journal of invertebrate pathology, 73(3): 309-314. insecticides and its management. JUNE 2017 29
Tabashnik, B.E., Morin, S., Unnithan, G.C., Yelich, A.J., Ellers-Kirk, whitefly (Bemisia tabaci) immunity and involves in Begomovirus C., Harpold, V.S., Sisterson, M.S., Ellsworth, P.C., Dennehy, T.J., acquisition. Scientific Reports, 6. Antilla, L. and Liesner, L., 2012. Sustained susceptibility of pink Wei, J., Guo, Y., Liang, G., Wu, K., Zhang, J., Tabashnik, B.E. bollworm to Bt cotton in the United States. GM crops & food, 3(3), and Li, X., 2015. Cross-resistance and interactions between Bt pp.194-200. toxins Cry1Ac and Cry2Ab against the cotton bollworm. Scientific Tabashnik, B.E., Wu, K. and Wu, Y., 2012b. Early detection of field- reports, 5, p.7714. evolved resistance to Bt cotton in China: cotton bollworm and pink Wei, Y., Wu, S., Yang, Y. and Wu, Y., 2017. Baseline Susceptibility of bollworm. J Invertebr Pathol 110:301–306. Field Populations of Helicoverpa armigera to Bacillus thuringiensis Tahir, M.N., Amin, I., Briddon, R.W. and Mansoor, S., 2011. The Vip3Aa Toxin and Lack of Cross-Resistance between Vip3Aa and merging of two dynasties—identification of an African cotton leaf Cry Toxins. Toxins, 9(4), p.127. curl disease-associated begomovirus with cotton in Pakistan. PLoS Wu, K., Liang, G. and Guo, Y., 1997. Phoxim resistance in One, 6(5), p.e20366. Helicoverpa armigera (Lepidoptera: Noctuidae) in China. Journal Tan, J., 1999. Mechanisms and genetics of resistance to fenvalerate of economic entomology, 90(4), pp.868-872. in cotton bollworm, Helicoverpa armigera (Huebner)(Lepidoptera: Xu, J., De Barro, P.J. and Liu, S.S., 2010. Reproductive Noctuidae) from China (Doctoral dissertation, University of incompatibility among genetic groups of Bemisia tabaci supports Reading). the proposition that the whitefly is a cryptic species complex. Bull Tanveer, M. and Mirza, M.B.1996. Effect of cotton leaf curl virus Entomol Res 100:359–366. on the yield components and fibre properties of four commercial Yang, Y., Li, Y., Wu, Y., 2013. Current Status of Insecticide Resistance varieties. Pak J Phytpath 8: 68-70. in Helicoverpa armigera After 15 Years of Bt Cotton Planting in Tay, W.T., Soria, M.F., Walsh, T., Thomazoni, D., Silvie, P., Behere, China. J Econ Entomol, 106: 375–381. G.T., Anderson, C. and Downes, S., 2013. A brave new world for an Youm, O., Sithanantham, S., Vaissayre, M., Nibouche, S., Martin, T., old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Ochou, G.O. and Momanyi, G., 2005. Bio-ecology and management Brazil. PLoS One, 8(11), p.e80134. of Helicoverpa for sustainable crop production in Africa. Tay, W.T., Walsh, T.K., Downes, S., Anderson, C., Jermiin, L.S., Zafar, Z.U., and Athar, H.U.R., 2013. Reducing disease incidence of Wong, T.K., Piper, M.C., Chang, E.S., Macedo, I.B., Czepak, C. cotton leaf curl virus (clcuv) in cotton (Gossypium hirsutum L.) by and Behere, G.T., 2017. Mitochondrial DNA and trade data support potassium supplementation. Pak. J. Bot. 45: 1029-38. multiple origins of Helicoverpa armigera (Lepidoptera, Noctuidae) in Brazil. Scientific Reports, 7. Zaidi, S.-E.-A., Iqbal, Z., Amin, I. and Mansoor, S., 2015. First report of Tomato leaf curl Gujarat virus, a bipartite begomovirus on Tuhan, N.C., Pawar, A.D., Arora, R.S., 1987. Use of Trichogramma cotton showing leaf curl symptoms in Pakistan. Plant Dis. 99, 1655. brasiliensis Ashmead against cotton bollworms in Srigangangar, doi: 10.1094/PDIS-02-15-0195-PDN Rajasthan, India. Journal of Advanced Zoology, 8(2):131-134 Zaidi, S.-E.-A., Shafiq, M., Amin, I., Scheffler, B.E., Scheffler, Van den Berg, H., Cock, M.J.W., Oduor, G.I. and Onsongo, E.K., J.A. and Briddon, R.W. 2016. Frequent Occurrence of Tomato 1993. Incidence of Helicoverpa armigera (Lepidoptera: Noctuidae) Leaf Curl New Delhi Virus in Cotton Leaf Curl Disease Affected and its natural enemies on smallholder crops in Kenya. Bulletin of Cotton in Pakistan. PLoS ONE 11: e0155520. Doi:10.1371/journal. Entomological Research, 83(03), pp.321-328. Pone.0155520 Editor: Baochuan Lin, Naval Research. Varma, A. and Malathi, V.G. 2003. Emerging geminiviruses Zaki, F.N., 1998. Efficiency of the entomopathogenic fungus, problems: A serious threat to crop production. Ann Appl Biol 142: Beauveria bassiana (Bals), against Aphis crassivora Koch and 145-64. Bemisia tabaci, Gennandius. Journal of Applied Entomology, 122(1- Varma, A., Malathi, V.G., Handa, A., Aiton, M., Harrison, B.D., 5), pp.397-399. Verma, J.P., Singh, R.P., Singh, M., Srivastava, M. and Singh, J., Zalucki, M.P., Daglish, G., Firempong, S., Twine, P.H., 1986. The 1993. Occurrence of leaf curl of cotton and okra in Northern India. biology and ecology of Helicoverpa armigera (H.ubner) and H. In: 6th International Congress of Plant Pathology, July 28-August 6, punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: what 1993, Montreal, Canada, 17.5.14. do we know? Aust. J. Zool. 34, 779–814. Vij, S., Pathak, D., Kaur, N., Pahwa, K. and Gill, M.S., 2016. Zalucki, M.P., Murray, D.A.H., Gregg, P.C., Fitt, G.P., Twine, P.H., Development and molecular confirmation of interspecific hybrids Jones, C., 1994. Ecology of Helicoverpa armigera (H.ubner) and H. between Gossypium hirsutum and Gossypium arboreum. Agricultural punctigera (Wallengren) in the inland of Australia: larval sampling Research Journal, 53(2), pp.169-172. and host plant relationships during winter and spring. Aust. J. Zool. Wan, P., Huang, Y., Wu, H., Huang, M., Cong, S., Tabashnik, B.E. 42, 329–346. and Wu, K., 2012. Increased frequency of pink bollworm resistance Zhang, H., Yin, W., Zhao, J., Jin, L., Yang, Y., Wu, S., Tabashnik, to Bt toxin Cry1Ac in China. PLoS One, 7(1), p.e29975. B.E. and Wu, Y., 2011. Early warning of cotton bollworm resistance Wan, P., Xu, D., Cong, S., Jiang, Y., Huang, Y., Wang, J., Wu, H., associated with intensive planting of Bt cotton in China. PLoS Wang, L., Wu, K., Carrière, Y. and Mathias, A., 2017. Hybridizing one, 6(8), p.e22874. transgenic Bt cotton with non-Bt cotton counters resistance in Zhou, X., Liu, Y., Robinson, D. J., and Harrison, B. D. 1998. Four pink bollworm. Proceedings of the National Academy of Sciences, DNA-A variants among Pakistani isolates of cotton leaf curl virus p.201700396. and their affinities to DNA-A of geminivirus isolates from okra. J. Wang, Z.Z., Shi, M., Huang, Y.C., Wang, X.W., Stanley, D. and Gen. Virol. 79, 915–923. doi: 10.1099/0022-1317-79-4-915. Chen, X.X., 2016. A peptidoglycan recognition protein acts in 30 ICAC RECORDER
Dr. David Matthias Stelly Winner of the ‘2017 ICAC Researcher of the Year Award’
The International Cotton Advisory Committee (ICAC) is (SNPs) for large-scale application, and also for targeted pleased to announce that Dr. David Matthias Stelly is the ICAC small-scale applications. He spearheaded formation of the Cotton Researcher of the Year for 2017. The ICAC honors a International “Cotton SNP Chip Consortium” and development leading cotton researcher each year by awarding a certificate of the “CottonSNP63K Array”, which enables high quality, of recognition, a shield and an honorarium of US$ 1,000. high-density SNP genotyping of Upland cottons. Dr Stelly Applications for the award were received from February 1 to created an isogenic Upland cotton platform for cytogenetic March 31, 2017. An independent panel of experts reviewed stock development and manipulation of Gossypium hirsutum the applications to select the winner. as well as interspecific “Chromosome Substitution”(CS) lines Dr. David M. Stelly is a Professor in the Department of Soil and their derivatives. Dr. Stelly has been involved with the & Crop Sciences at Texas A&M University and Texas A&M international development of cotton structural genomics from AgriLife Research. A world-renowned geneticist and cotton the outset. He was among the key contributors to high-quality breeder, Dr Stelly started his plant research career in the assemblies of the D5 genome of Gossypium raimondii, the extant Peruvian wild diploid cotton in 2012, and the (AD) 1970s. He has a BS degree in Genetics from the University of 1 Wisconsin (UW). He completed a MS in Plant Breeding and genome assembly for Upland cotton reported in 2015. These Cytogenetics in 1979 at Iowa State University and a PhD in advances are leading to transformations in multiple scientific Plant Breeding and Plant Genetics at UW in 1983. He joined and applied disciplines of cotton. He has authored and co- Texas A&M in 1983. authored over 150 formal publications. Dr. Stelly has over 30 years of professional experience Dr. Stelly is Chair of the International Cotton Genome and leadership in plant breeding of cotton with expertise Initiative, formerly President of the National Association of on germplasm introgression, reproductive biology and Plant Breeders (NAPB), external reviewer of the USDA’s cytology, cytogenetics, genetic and genomics. His scientific Plant Genetic Resources, Genomics and Genetic Improvement endeavors entail a broad spectrum of wild species germplasm, program, member of International Organizing Committee for introgression methods, chromosome substitution, ploidy WCRC-6, and the National Academy of Sciences GE Crops manipulations, conventional cytogenetics and fluorescence Committee. He has twice received the Cotton Genetic Research in situ hybridization (FISH), genetic analysis, SSR and SNP Award, and recently became a Fellow of the Crop Science marker development, genotyping, genome and trait mapping, Society of America, and received the Lifetime Achievement marker assisted selection, reproductive cytology and genetics, Award from the University Agricultural Sciences Dharwad, various types of genome mapping (linkage, BAC physical, India. radiation hybrid), genomics, sequencing and their integration. Further information about the ICAC Researcher of the Year Dr. Stelly has revolutionized global cotton research capabilities Award can be found at https://www.icac.org/tech/ICAC- by enabling global use of single-nucleotide polymorphisms Researcher-of-the-Year-Award. JUNE 2017 31
International Cotton Researchers Association (ICRA): Updates on Major Activities Michel Fok, Chair, ICRA
ICRA Secretariat Australia (1994), WCRC2 in Greece (1998) and WCRC3 in After the election of a new Executive Committee in 2016, South Africa (2003) are available only in hard copy. ICRA has ICRA initiated a process in May 2016 to identify an institution now launched an initiative to coordinate the availability of full that could serve as its Secretariat. As described in the previous papers of all the WCRC conferences held so far on its website. issue of THE ICAC RECORDER, six cotton-related institutions The objective is to provide the papers in one place to maintain from Latin America, Asia and Africa offered to undertake the an active interaction on global knowledge and scientific responsibility of serving as the Secretariat. The Executive advances on cotton. This would ensure the availability of Committee appreciated the show of interest from each of the all WCRC papers on the ICRA website as a permanent institutions, and there was agreement that all applicants were online free-access repository, irrespective of the status of the highly qualified. An offer from the Pakistan Central Cotton individual conference websites. ICRA now has access to the Committee (PCCC) electronic files of all communications and full papers of all the to act as ICRA previous conferences starting from WCRC1. ICRA received Secretariat for five excellent support from the organizers of the previous WCRC years was accepted conferences in setting up the online proceedings on the ICRA by the Executive website. The online proceedings of the WCRC1 are now Committee during ready, and it is worth visiting the 1994 panorama of cotton its meeting in research in the world. Islamabad in November 2016. Executive Committee The PCCC will soon According to the ICRA Rules and bylaws, ICAC is endowed announce the names with one seat in the ICRA Executive Committee, occupied of Secretary and by the Head of its Technical Information Section. After Dr Assistant Secretary Rafiq’s retirement, ICAC is now represented by Dr. Keshav of the Secretariat. Kranthi. The process has now On April 3, 2017, Dr Rafiq Chaudhry retired as the Head, reached the final stage of signing the official Memorandum Technical information Section of the ICAC after serving for of Understanding (MoU). A formal ceremony could take a marathon-like 26 dedicated years. ICRA was his brainchild. place soon in Pakistan. Dr. Khalid Abdullah, Vice-President, Rafiq, as researchers across the world fondly call him, not only Pakistan Central Cotton Committee (khalidabdullah99@ gave shape to the idea of ICRA by laying a firm foundation, yahoo.com) and Dr. Michel Fok Ah Chuen, Chairman, ICRA but also by setting up a roadmap to nurture it. He was deeply will be signatories to the MoU. convinced for the need of ICRA as a global knowledge- sharing platform. Rafiq managed to have ICAC provide its Setting Up Full Paper Proceedings support to set up ICRA and also made use of his international network to help set up the Executive Committee of ICRA with of the WCRC1 to WCRC6 on a sound geographical representation. Readers of THE ICAC ICRA Web Page RECORDER and members of ICRA fondly acknowledge Starting from the WCRC4 in Lubbock USA in 2007, each his vision and perseverance in setting up ICRA as a global of the conferences created their own dedicated web sites platform for cotton researchers. for WCRC5 in Mumbai, India, in 2011 and for WCRC6 in Goiania, Brazil, in 2016. Online submission of abstracts, ICRA Platform registration etc., was done on the websites. Proceedings of ICRA has invested substantial time and effort to restructure the conferences were also uploaded online on the WCRC its website to facilitate scientific interaction among members. websites. These specific websites could be accessed for a ICRA provides an opportunity for researchers to exchange limited period of time on their respective online locations, and notes, views and communications on the ICRA website based each is now unavailable. on the online proceedings. Each communication is presented However, efforts were made to maintain the full research as a newly tagged post, and by default becomes a topic in the paper proceedings of the conferences on the ICAC website. discussion forum that any visitor can follow. ICRA members Proceeding papers of the first three conferences WCRC1 in can contribute through comments and questions. Any ICRA 32 ICAC RECORDER member can submit posts, which are moderated before the published on the ICRA website. topics are listed for forum discussion. Members can launch The ICRA platform is now almost ripe to be fully utilized new forum topics not linked to posts, without moderation. by researchers to prepare for a virtual world of togetherness. The profile function has been enriched to enable the members There is a need to take full advantage of the ICRA website to inform about their projects and publications in addition to share ideas and thoughts on cotton science for the sake to their affiliation and background. A Wiki function named of the world cotton sector. Researchers may send their ideas Gossypedia has been added with an objective to provide a to [email protected] to improve the website or the platform for the transfer of knowledge between different functioning of ICRA so that it can become a vibrant forum generations of cotton researchers. More information on the for exchange of knowledge amongst cotton researchers of the above mentioned functions is available through various posts world.
ACRDN VII Meeting ASIAN COTTON RESEARCH AND DEVELOPMENT NETWORK (ACRDN)
Venue: Le Méridien, Nagpur, India 15-17 September 2017 Agenda: Theme: ‘Production of Quality Fiber and Doubling Farmers • Discuss global best practices for yield enhancement Income’ • Develop sustainable action plan to manage whiteflies, Sponsors: ICAC & ISCI (Indian Society for Cotton pink bollworm, leaf curl virus and the American bollworm Improvement) • Discuss recent research developments, technologies and Hosts: gaps • Indian Society for Cotton Improvement (ISCI), Mumbai Contacts: & • Dr. C. D. Mayee, President ISCI: • Indian Council of Agricultural Research (ICAR), New [email protected] Delhi • Dr. A. J. Shaikh, Secretary, ISCI: Participants: 50-60 including 25-30 overseas delegates [email protected] Speakers: 15-16 invited experts on latest technological • Dr. M. V. Venugopalan, organizing secretary, ACRDN: developments [email protected] • Dr. Keshav R. Kranthi, ICAC: [email protected]
ALIDA XIV Meeting LATIN AMERICAN ASSOCIATION FOR COTTON RESEARCH AND DEVELOPMENT (ALIDA)
• Develop area-wide IPM implementation plan Venue: Hoilday Inn Express de Maceió Brazil, 28th August 2017. • Discuss recent research developments, technologies and gaps Theme: ‘Boll Weevil Integrated Pest Management’ Contacts: Sponsors: ICAC & FAO • Dr. Sebastiao Barbosa, EMBRAPA: Host: EMBRAPA [email protected] Participants: 25-30 • Dr. Adriana Gregolin, FAO: Speakers: 5-6 invited experts on latest technological [email protected] developments • Dr. Keshav R. Kranthi, ICAC: Agenda: [email protected] • IPM recommendations for sustainable cotton with emphasis on Boll weevil management